A cyclic peptide inhibitor of C-terminal binding protein dimerization links metabolism with mitotic fidelity in breast cancer cells
Open accessAbstract
Identification of direct modulators of transcription factor protein–protein interactions is a key challenge for ligand discovery that promises to significantly advance current approaches to cancer therapy. Here, we report an inhibitor of NADH-dependent dimerization of the C-terminal binding protein (CtBP) transcriptional repressor, identified by screening genetically encoded cyclic peptide libraries of up to 64 million members. CtBP dimers form the core of transcription complexes associated with epigenetic regulation of multiple genes that control many characteristics of cancer cells, including proliferation, survival and migration. CtBP monomers also have distinct and critical cellular function, thus current experimental tools that deplete all forms of a targeted protein (e.g. siRNA) do not allow the cellular consequences of this metabolically regulated transcription factor to be deciphered. The most potent inhibitor from our screen (cyclo-SGWTVVRMY) is demonstrated to disrupt CtBP dimerization in vitro and in cells. This compound is used as a chemical tool to establish that the NADH-dependent dimerization of CtBPs regulates the maintenance of mitotic fidelity in cancer cells. Treatment of highly glycolytic breast cancer cell lines with the identified inhibitor significantly reduced their mitotic fidelity, proliferation and colony forming potential, whereas the compound does not affect mitotic fidelity of cells with lower glycolytic flux. This work not only links the altered metabolic state of transformed cells to a key determinant of the tumor cell phenotype, but the uncovered compound also serves as the starting point for the development of potential therapeutic agents that target tumors by disrupting the CtBP chromatin-modifying complex.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Hallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590 · see citing works
Understanding the Warburg Effect: The Metabolic Requirements of Cell Proliferation
Vander Heiden, M. G., Cantley, L. C., & Thompson, C. B. (2009) · Science · doi:10.1126/science.1160809 · Cited by 16,197 · see citing works
Aerobic glycolysis: Meeting the metabolic requirements of cell proliferation
Lunt, S. Y., & Vander Heiden, M. G. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-092910-154237 · Cited by 3,057 · see citing works
Reaching for high-hanging fruit in drug discovery at protein–protein interfaces
Wells, J. A., & McClendon, C. L. (2007) · Nature · doi:10.1038/nature06526 · Cited by 1,963 · see citing works
Evidence that glutamine, not sugar, is the major energy source for cultured HeLa cells.
Reitzer, L. J., Wice, B. M., & Kennell, D. (1979) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)30124-2 · Cited by 1,240 · see citing works
Transcription factors as targets for cancer therapy
Darnell, J. E. (2002) · Nature Reviews Cancer · doi:10.1038/nrc906 · Cited by 1,194 · see citing works
Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis
Holland, A. J., & Cleveland, D. W. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2718 · Cited by 859 · see citing works
Coordinated histone modifications mediated by a CtBP co-repressor complex
Shi, Y. G., Sawada, J.-I., Sui, G., Affar, E. B., Whetstine, J. R., Lan, F., Ogawa, H., Luke, M. P.-S., Nakatani, Y., & Shi, Y. (2003) · Nature · doi:10.1038/nature01550 · Cited by 799 · see citing works
Impaired DNA Damage Response, Genome Instability, and Tumorigenesis in SIRT1 Mutant Mice
Wang, R.-H., Sengupta, K., Li, C., Kim, H., Cao, L., Xiao, C., Kim, S., Xu, X., Yin, Z., Chilton, B. S., et al. (2008) · Cancer Cell · doi:10.1016/j.ccr.2008.09.001 · Cited by 769 · see citing works
Direct inhibition of the NOTCH transcription factor complex
Moellering, R. E., Cornejo, M., Davis, T. N., Bianco, C. D., Aster, J. C., Blacklow, S. C., Kung, A. L., Gilliland, D. G., Verdine, G. L., & Bradner, J. E. (2009) · Nature · doi:10.1038/nature08543 · Cited by 752 · see citing works
The NAD metabolome — a key determinant of cancer cell biology
Chiarugi, A., Dölle, C., Felici, R., & Ziegler, M. (2012) · Nature reviews. Cancer · doi:10.1038/nrc3340 · Cited by 645 · see citing works
SIRT2 Maintains Genome Integrity and Suppresses Tumorigenesis through Regulating APC/C Activity
Kim, H., Vassilopoulos, A., Wang, R.-H., Lahusen, T. J., Xiao, Z., Xu, X., Li, C., Veenstra, T. D., Li, B., Yu, H., et al. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.09.004 · Cited by 536 · see citing works
Zheng, L., Roeder, R. G., & Luo, Y. (2003) · Cell · doi:10.1016/s0092-8674(03)00552-x · Cited by 534 · see citing works
Lkb1 regulates cell cycle and energy metabolism in haematopoietic stem cells
Nakada, D., Saunders, T. L., & Morrison, S. J. (2010) · Nature · doi:10.1038/nature09571 · Cited by 524 · see citing works
CtBP, an Unconventional Transcriptional Corepressor in Development and Oncogenesis
Chinnadurai, G. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00443-4 · Cited by 523 · see citing works
Roles of p53, MYC and HIF-1 in regulating glycolysis–the seventh hallmark of cancer
Yeung, S. J., Pan, J., & Lee, M.-H. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8224-x · Cited by 514 · see citing works
Production of cyclic peptides and proteins <i>in vivo</i>
Scott, C. P., Abel-Santos, E., Wall, M., Wahnon, D. C., & Benkovic, S. J. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.24.13638 · Cited by 402 · see citing works
Fjeld, C. C., Birdsong, W. T., & Goodman, R. H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1633591100 · Cited by 313 · see citing works
Hildebrand, J. D., & Soriano, P. M. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.15.5296-5307.2002 · Cited by 301 · see citing works
Transcription Corepressor CtBP Is an NAD+-Regulated Dehydrogenase
Kumar, V., Carlson, J. E., Ohgi, K. A., Edwards, T. A., Rose, D. W., Escalante, C. R., Rosenfeld, M. G., & Aggarwal, A. K. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00650-0 · Cited by 299 · see citing works
The Transcriptional Corepressor CtBP: A Foe of Multiple Tumor Suppressors
Chinnadurai, G. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-3349 · Cited by 265 · see citing works
Protein–protein interaction inhibitors get into the groove
Mullard, A. (2012) · Nature Reviews Drug Discovery · doi:10.1038/nrd3680 · Cited by 246 · see citing works
The engine driving the ship: metabolic steering of cell proliferation and death
Buchakjian, M. R., & Kornbluth, S. A. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2972 · Cited by 215 · see citing works
Redox sensor CtBP mediates hypoxia-induced tumor cell migration
Zhang, Q., Wang, S.-Y., Nottke, A. C., Rocheleau, J. V., Piston, D. W., & Goodman, R. H. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603269103 · Cited by 200 · see citing works
Nardini, M., Spanò, S., Cericola, C., Pesce, A., Massaro, A., Millo, E., Luini, A., Corda, D., & Bolognesi, M. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg283 · 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-citationAlmeida, A., Bolaños, J. P., & Moncada, S. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0913668107 · Cited by 166 · see citing works
Tavassoli, A., Lu, Q., Gam, J., Pan, H., Benkovic, S. J., & Cohen, S. N. (2008) · ACS Chemical Biology · doi:10.1021/cb800193n · Cited by 153 · see citing works
Self-citationDi, L. J., Byun, J. S., Wong, M., Wakano, C., Taylor, T. J., Bilke, S., Baek, S., Hunter, K. W., Yang, H. H., Lee, M. Y., et al. (2013) · Nature Communications · doi:10.1038/ncomms2438 · Cited by 152 · see citing works
The multiple activities of CtBP/BARS proteins: the Golgi view
Corda, D., Colanzi, A., & Luini, A. (2006) · Trends in Cell Biology · doi:10.1016/j.tcb.2006.01.007 · Cited by 142 · see citing works
CtBP represses p300-mediated transcriptional activation by direct association with its bromodomain
Kim, J.-H., Cho, E., Kim, S., & Youn, H. (2005) · Nature Structural & Molecular Biology · doi:10.1038/nsmb924 · Cited by 122 · see citing works
Inhibition of transcription factors with small organic molecules
Berg, T. (2008) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2008.07.023 · Cited by 115 · 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
Mazurek, S., Michel, A., & EIGENBRODT, E. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.8.4941 · Cited by 105 · see citing works
Quinlan, K. G. R., Nardini, M., Verger, A., Francescato, P., Yaswen, P., Corda, D., Bolognesi, M., & Crossley, M. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.00680-06 · Cited by 102 · see citing works
Rheostat Control of Gene Expression by Metabolites
Ladurner, A. G. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.09.002 · Cited by 95 · see citing works
Genetically 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-citationHdm2 Recruits a Hypoxia-Sensitive Corepressor to Negatively Regulate p53-Dependent Transcription
Mirnezami, A., Campbell, S. J., Darley, M., Primrose, J. M., Johnson, P., & Blaydes, J. P. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00454-8 · Cited by 91 · see citing works
Self-citationTherapeutic targeting of C-terminal binding protein in human cancer
Straza, M. W., Paliwal, S., Kovi, R. C., Rajeshkumar, B. R., Trenh, P., Parker, D., Whalen, G. F., Lyle, S. R., Schiffer, C. A., & Grossman, S. R. (2010) · Cell Cycle · doi:10.4161/cc.9.18.12936 · Cited by 86 · see citing works
Bhambhani, C., Chang, J. L., Akey, D. L., & Cadigan, K. M. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.100 · Cited by 72 · 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-citationAMPK: Evidence for an energy-sensing cytokinetic tumor suppressor
Vázquez‐Martín, A., Oliveras‐Ferraros, C., López‐Bonet, E., & Menéndez, J. A. (2009) · Cell Cycle · doi:10.4161/cc.8.22.9905 · Cited by 66 · see citing works
Zhao, L., Kuppuswamy, M. N., Vijayalingam, S., & Chinnadurai, G. (2009) · BMC Molecular Biology · doi:10.1186/1471-2199-10-89 · Cited by 66 · see citing works
C-terminal binding proteins: Emerging roles in cell survival and tumorigenesis
Bergman, L., & Blaydes, J. P. (2006) · APOPTOSIS · doi:10.1007/s10495-006-6651-4 · Cited by 62 · see citing works
Self-citationAchouri, Y., Noël, G., & SCHAFTINGEN, E. V. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.11.111 · Cited by 58 · see citing works
CtBPs Promote Cell Survival through the Maintenance of Mitotic Fidelity
Bergman, L., Birts, C. N., Darley, M., Gabrielli, B. G., & Blaydes, J. P. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.00439-09 · Cited by 53 · see citing works
Self-citationBergman, L., Morris, L. R., Darley, M., Mirnezami, A., Gunatilake, S. C., & Blaydes, J. P. (2006) · BMC Cell Biology · doi:10.1186/1471-2121-7-35 · Cited by 37 · see citing works
Self-citationC-terminal binding protein maintains mitochondrial activities
Kim, J., & Youn, H. (2009) · Cell Death and Differentiation · doi:10.1038/cdd.2008.186 · Cited by 32 · see citing works
CtBPs promote mitotic fidelity through their activities in the cell nucleus
Birts, C. N., Bergman, L., & Blaydes, J. P. (2010) · Oncogene · doi:10.1038/onc.2010.507 · Cited by 11 · see citing works
Self-citationIncapacitating CtBP to kill cancer
Zhao, L.-Z., & Chinnadurai, G. (2010) · Cell Cycle · doi:10.4161/cc.9.18.13221 · Cited by 7 · see citing works
A new layer of regulation is required to silence the DNA damage checkpoint
Wang, Y. (2010) · Cell Cycle · doi:10.4161/cc.9.18.13180 · Cited by 1 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [1]Darnell JE Jr Nat Rev Cancer 2002 2 740 12360277
- [14]Vazquez-Martin A Oliveras-Ferraros C Lopez-Bonet E Menendez JA Cell Cycle 2009 8 3679 19844168
Cited by
Sorted by citations
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
RNA Display Methods for the Discovery of Bioactive Macrocycles
Huang, Y., Wiedmann, M. M., & Suga, H. (2018) · Chemical Reviews · doi:10.1021/acs.chemrev.8b00430 · Cited by 309 · 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-citationCardote, 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-citationMacrocycles as protein–protein interaction inhibitors
Dougherty, P. G., Qian, Z., & Pei, D. (2017) · Biochemical Journal · doi:10.1042/bcj20160619 · Cited by 179 · see citing works
Conformational Control of Macrocycles by Remote Structural Modification
Appavoo, S. D., Huh, S., Diaz, D. B., & Yudin, A. K. (2019) · Chemical Reviews · doi:10.1021/acs.chemrev.8b00742 · Cited by 157 · see citing works
A 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-citationSICLOPPS 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-citationShen, Y., Kapfhamer, D., Minnella, A. M., Kim, J.-E., Won, S. J., Chen, Y., Huang, Y., Low, L. H., Massa, S. M., & Swanson, R. A. (2017) · Nature Communications · doi:10.1038/s41467-017-00707-0 · Cited by 133 · 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
The Role of CtBP1 in Oncogenic Processes and Its Potential as a Therapeutic Target
Blevins, M. A., Huang, M., & Zhao, R. (2017) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-16-0592 · Cited by 114 · see citing works
Improving Accuracy, Diversity, and Speed with Prime Macrocycle Conformational Sampling
Sindhikara, D., Spronk, S. A., Day, T., Borrelli, K. W., Cheney, D. L., & Posy, S. (2017) · Journal of Chemical Information and Modeling · doi:10.1021/acs.jcim.7b00052 · Cited by 113 · see citing works
Dcona, M. M., Morris, B. L., Ellis, K. C., & Grossman, S. R. (2017) · Cancer Biology & Therapy · doi:10.1080/15384047.2017.1323586 · Cited by 102 · see citing works
Directing evolution: the next revolution in drug discovery?
Davis, A. M., Plowright, A. T., & Valeur, E. (2017) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2017.146 · Cited by 86 · see citing works
Cyclic Peptides for the Treatment of Cancers: A Review
Ramadhani, D., Maharani, R., Gazzali, A. M., & Muchtaridi, M. (2022) · Molecules · doi:10.3390/molecules27144428 · Cited by 80 · 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-citationTargeting protein−protein interfaces using macrocyclic peptides
Gao, M., Cheng, K., & Yin, H. H. (2015) · Biopolymers · doi:10.1002/bip.22625 · Cited by 72 · see citing works
Birts, C. N., Banerjee, A., Darley, M., Dunlop, C. R., Nelson, S., Nijjar, S. K., Parker, R., West, J. J., Tavassoli, A., Rose-Zerilli, M. J. J., et al. (2020) · Science Signaling · doi:10.1126/scisignal.aau9529 · Cited by 56 · see citing works
Self-citationBlevins, M. A., Kouznetsova, J., Krueger, A. B., King, R., Griner, L. A. M., Hu, X., Southall, N. T., Marugán, J., Zhang, Q., Ferrer, M., et al. (2014) · SLAS DISCOVERY · doi:10.1177/1087057114561400 · Cited by 55 · see citing works
Korwar, S., Morris, B. L., Parikh, H. I., Coover, R. A., Doughty, T. W., Love, I. M., Hilbert, B. J., Royer, W. E., Kellogg, G. E., Grossman, S. R., et al. (2016) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2016.04.037 · Cited by 50 · see citing works
Structure-Guided Design of a High Affinity Inhibitor to Human CtBP
Hilbert, B. J., Morris, B. L., Ellis, K. C., Paulsen, J. L., Schiffer, C. A., Grossman, S. R., & Royer, W. E. (2015) · ACS Chemical Biology · doi:10.1021/cb500820b · Cited by 47 · see citing works
Tackling Undruggable Targets with Designer Peptidomimetics and Synthetic Biologics
Swenson, C., Mandava, G., Thomas, D. M., & Moellering, R. E. (2024) · Chemical Reviews · doi:10.1021/acs.chemrev.4c00423 · Cited by 48 · 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
González‐Muñiz, R., Bonache, M. Á., & de Vega, M. J. P. (2021) · Molecules · doi:10.3390/molecules26020445 · Cited by 43 · see citing works
Banerjee, A., Birts, C. N., Darley, M., Parker, R., Mirnezami, A. H., West, J. J., Cutress, R., Beers, S. A., Rose-Zerilli, M. J. J., & Blaydes, J. P. (2018) · Carcinogenesis · doi:10.1093/carcin/bgy174 · Cited by 42 · see citing works
Self-citationMethods 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-citationTraceless Production of Cyclic Peptide Libraries in E. coli
Townend, J., & Tavassoli, A. (2016) · ACS Chemical Biology · doi:10.1021/acschembio.6b00095 · Cited by 38 · see citing works
Self-citationThe transrepression and transactivation roles of CtBPs in the pathogenesis of different diseases
Chen, Z. (2021) · Journal of Molecular Medicine · doi:10.1007/s00109-021-02107-w · Cited by 28 · see citing works
Leitch, E. K., Elumalai, N., Fridén‐Saxin, M., Dahl, G., Wan, P., Clarkson, P. N., Valeur, E., Pairaudeau, G., Boyd, H., & Tavassoli, A. (2018) · Chemical Science · doi:10.1039/c8sc01186a · Cited by 26 · see citing works
Self-citationAndrews, A.-L., Nordgren, I. K., Campbell-Harding, G., Holloway, J. W., Holgate, S. T., Davies, D. E., & Tavassoli, A. (2013) · Molecular BioSystems · doi:10.1039/c3mb70298g · Cited by 26 · see citing works
Self-citationLi, C., Xiao, X., Qian, Y.-H., & Zhou, Z. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.28802 · Cited by 24 · see citing works
Elduque, X., Pedroso, E., & Grandas, A. (2014) · The Journal of Organic Chemistry · doi:10.1021/jo500427c · Cited by 22 · see citing works
Deng, Y., Guo, W., Li, G., Li, S., Li, H., Li, X., Niu, B., Song, M., Zhang, Y., Xu, Z., et al. (2020) · Journal of Breast Cancer · doi:10.4048/jbc.2020.23.e7 · Cited by 21 · see citing works
CtBP2 proteome: Role of CtBP in E2F7-mediated repression and cell proliferation
Zhao, L., Subramanian, T., Vijayalingam, S., & Chinnadurai, G. (2014) · Genes & Cancer · doi:10.18632/genesandcancer.2 · Cited by 19 · see citing works
Intracellular Production of Cyclic Peptide Libraries with SICLOPPS
Osher, E. L., & Tavassoli, A. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-6451-2_3 · Cited by 18 · see citing works
Self-citationCui, L., Liu, W., Liu, H., Qin, Q., Wu, S., He, S., Zhang, Z., Pang, X., & Zhu, C. (2020) · International Journal of Nanomedicine · doi:10.2147/ijn.s252769 · Cited by 16 · see citing works
Conformational Plasticity of Cyclic Ras‐Inhibitor Peptides Defines Cell Permeabilization Activity
Takeuchi, K., Imai, M., Tokunaga, Y., Fujisaki, M., Kamoshida, H., Takizawa, T., Hanzawa, H., & Shimada, I. (2021) · Angewandte Chemie International Edition · doi:10.1002/anie.202016647 · Cited by 16 · see citing works
A bidirectional fluorescent two-hybrid system for monitoring protein–protein interactions
Nordgren, I. K., & Tavassoli, A. (2013) · Molecular BioSystems · doi:10.1039/c3mb70438f · Cited by 16 · see citing works
Self-citationGenetically Encoded Cyclic Peptide Libraries: From Hit to Lead and Beyond
Valentine, J., & Tavassoli, A. (2018) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2018.09.020 · Cited by 14 · see citing works
Self-citationErlandsen, H., Jecrois, A. M., Nichols, J. C., Cole, J. L., & Royer, W. E. (2022) · FEBS Letters · doi:10.1002/1873-3468.14276 · Cited by 13 · see citing works
CtBP represses Dpp signaling as a dimer
Bi, C., Meng, F., Yang, L., Cheng, L. Z., Wang, P., Chen, M., Fang, M., & Xie, H. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.12.018 · Cited by 12 · see citing works
HIF-1 promotes the expression of its α-subunit via an epigenetically regulated transactivation loop
Asby, D. J., Cuda, F., Hoakwie, F., Miranda, E., & Tavassoli, A. (2014) · Molecular BioSystems · doi:10.1039/c4mb00351a · Cited by 11 · see citing works
Self-citationThe effects of restricted glycolysis on stem-cell like characteristics of breast cancer cells
Banerjee, A., Arvinrad, P., Darley, M., Laversin, S. A., Parker, R., Rose-Zerilli, M. J. J., Townsend, P. A., Cutress, R., Beers, S. A., Houghton, F. D., et al. (2018) · Oncotarget · doi:10.18632/oncotarget.25299 · Cited by 11 · see citing works
Self-citationEpigenetic re-wiring of breast cancer by pharmacological targeting of C-terminal binding protein
Byun, J. S., Park, S., Yi, D. I., Shin, J., Gil‐Hernández, S., Hewitt, S. M., Nicklaus, M. C., Peach, M. L., Guasch, L., Tang, B., et al. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1892-7 · Cited by 11 · see citing works
Identification and characterization of a new potent inhibitor targeting CtBP1/BARS in melanoma cells
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-024-03044-5 · Cited by 8 · see citing works
Chen, X., Zhang, W., Zhang, Q., Song, T., Yu, Z., Li, Z., Duan, N., & Dang, X. (2020) · PubMed Central · doi:10.14348/molcells.2020.0042 · Cited by 8 · see citing works
Kreuzer, M., Banerjee, A., Birts, C. N., Darley, M., Tavassoli, A., Ivan, M., & Blaydes, J. P. (2020) · FEBS Letters · doi:10.1002/1873-3468.13874 · Cited by 8 · see citing works
Self-citationShen, Q., Zhang, C., Liu, H., Liu, Y., Cao, J., Zhang, X., Liang, Y. J., Zhao, M., & Lai, L. (2016) · MedChemComm · doi:10.1039/c5md00549c · Cited by 4 · see citing works
A new method for network bioinformatics identifies novel drug targets for mucinous ovarian carcinoma
Craig, O., Lee, S., Pilcher, C., Saoud, R., Abdirahman, S. M., Salazar, C., Williams, N. P., Ascher, D. B., Vary, R., Luu, J., et al. (2024) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqae096 · Cited by 3 · see citing works
Castillo, F., & Tavassoli, A. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9504-2_15 · Cited by 3 · see citing works
Self-citationDrug Design Methods to Regulate Protein–Protein Interactions
Poluri, K. M., Gulati, K., Tripathi, D. K., & Nagar, N. (2023) · Springer eBooks · doi:10.1007/978-981-99-2423-3_6 · Cited by 2 · see citing works
Macrocyclic peptides as protein–protein interaction modulators: a review
Sunny, E. A. S., & Sadanandan, S. (2026) · Organic & Biomolecular Chemistry · doi:10.1039/d6ob00106h · Cited by 2 · see citing works
Conformational Plasticity of Cyclic Ras‐Inhibitor Peptides Defines Cell Permeabilization Activity
Takeuchi, K., Imai, M., Tokunaga, Y., Fujisaki, M., Kamoshida, H., Takizawa, T., Hanzawa, H., & Shimada, I. (2021) · Angewandte Chemie · doi:10.1002/ange.202016647 · Cited by 1 · see citing works
Hilbert, B. J. (2013) · eScholarship@UMassChan · doi:10.13028/m23k66
Macrocycles for Protein–Protein Interactions
Leitch, E. K., & Tavassoli, A. (2017) · doi:10.1002/9781119092599.ch8
Self-citationCell-based assays for identifying, validating and optimizing protein–protein interaction modulators
Male, A. L., & Tavassoli, A. (2013) · doi:10.4155/ebo.13.348
Self-citationFoster, A. D., Chung, C., Hann, M. M., Simpson, G. L., & Tavassoli, A. (2020) · Peptide Science · doi:10.1002/pep2.24178
Self-citationTakeuchi, K. (2022) · Royal Society of Chemistry eBooks · doi:10.1039/9781839165702-00411
An Insight into Synthesis and Biological Evaluation of Anti-breast Cancer Peptides
Gupta, D., Yadav, S., Kumari, B., & Kumar, S. (2025) · Current Cancer Therapy Reviews · doi:10.2174/0115733947328950241101173253
Liu, Y., Kuo, W., Lo, C., Huang, C., Lee, M.-S., Chang, J., Hsieh, C., & Hsiao, F. (2025) · Behavioral Sciences · doi:10.3390/bs15070940
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25763070
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716396
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716393
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716360
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716357
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716378
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716414
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716384
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716363
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716411
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716402
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716390
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716372
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716405
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716408
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716366
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25762968
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716381
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716399
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716387
Filograna, A., Tito, S. D., Monte, M. L., Oliva, R., Bruzzese, F., Roca, M. S., Zannetti, A., Greco, A., Spano, D., Ayala, I., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26716375
Acar, E., Başağa, H., Timuçin, E., & Timuçin, A. C. (2026) · ACS Omega · doi:10.1021/acsomega.6c01122
Yang, L., Behera, A., Meyers, H. J., & Wang, T. (2026) · ChemBioChem · doi:10.1002/cbic.70532
BindingDB Entry 6854: Structure-guided design of a high affinity inhibitor to human CtBP.
BindingDB (2015) · UC San Diego · doi:10.7270/q2416vtk
- Authors
- Birts, C. N., Nijjar, S. K., Mardle, C. A., Hoakwie, F., Duriez, P. J., Blaydes, J. P., & Tavassoli, A.
- Affiliations
- University of Southampton (GB)
- Corresponding author
- Blaydes, Jeremy P.
- Tavassoli, Ali
- Venue
- Chemical Science
- Publisher
- Royal Society of Chemistry (RSC)
- Published
- 2013
- Volume
- 4
- Issue
- 8
- Pages
- 3046
- ISSN
- 2041-6520 (ISSN-L)
- 2041-6539
- PMC
- PMC6237275
- OpenAlex
- W2107087021
- Cited by
- 85
- References
- 51
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 24 · 2023: 1 · 2022: 3 · 2021: 5 · 2020: 7 · 2019: 4 · 2018: 6 · 2017: 9 · 2016: 4 · 2015: 4 · 2014: 8 · 2013: 5
- FWCI
- 3.29
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Chemical Science (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- ePrints Soton (University of Southampton) (acceptedVersion)
- Funders
- Cancer Research UK (A10263)
- Breast Cancer Campaign
- University of Southampton
- Directorate for Biological Sciences
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chemical Synthesis and Analysis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Keywords
- CtBP, cyclic peptide inhibitors, protein-protein interaction, mitotic fidelity, breast cancer, glycolysis, cancer metabolism, transcriptional repressor, epigenetic regulation, chromatin-modifying complexes, chemical probes, cell proliferation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
