Publications - Heddle Lab

2024
- Norbert Osiński, Karolina Majsterkiewicz, Zuzanna Pakosz-Stępień, Yusuke Azuma, Artur P. Biela, Szymon Gaweł, Jonathan G. Heddle. Designed, Programmable Protein Cages Utilizing Diverse Metal Coordination Geometries Show Reversible, pH-Dependent Assembly.
  In: Marcomolecular Rapid Communications. 2024
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- Michalczyk, E., Pakosz-Stepień, Z., Liston, J., Ghilarov, D., Gittins, O., Pabis, M., Heddle, J., Ghilarov, D. Structural basis of chiral wrap and T-segment capture by Escherichia coli DNA gyrase.
  In: PNAS. 2024
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- Wilkens, G., Stepien, P., Sakai, Y., Sirajul Islam, M., Heddle, G. A DNA Origami Bubble Blower for Liposome Production.
  In: ACS Omega. 2024
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- Lin, T., Kleenmann, L., Jeżowski, J., Dobosz, D., Rawski, M., Indyka, P., Ważny, G., Mehta, R., Chramiec-Głąbik, A., Koziej, L., Ranff, T., Fufezan, C., Wawro, M., Kochan, J., Bereta, J., Leidel, S.A., Glatt, S. The molecular basis of tRNA selectivity by human pseudouridine synthase 3.
  In: Molecular Cell. 2024
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- Michalczyk, E., Pabis, M., Heddle, J., Ghilarov D. Structure of Escherichia coli DNA gyrase with chirally wrapped DNA supports ratchet-and-pawl mechanism for ATP-powered supercoiling motor.
  In: Biorxiv 2024 [Preprint]
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- Naskalska A, Heddle JG. Virus-like particles derived from bacteriophage MS2 as antigen scaffolds and RNA protective shells.
  In: Nanomedicine (Lond). 2024
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- Stupka I, Biela AP, Piette B, Kowalczyk A, Majsterkiewicz K, Borzęcka-Solarz K, Naskalska A, Heddle JG. An artificial protein cage made from a 12-membered ring.
  In: J Mater Chem B. 2024 J
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- Gaweł S., Naskalska A.,Osiński N., Heddle J.G. Running rings around protein cages: case study of artificial TRAP cages.
  In: Amino Acids, Peptides and Proteins, 2024
2023
- Stępień P, Świątek S, Robles MYY, Markiewicz-Mizera J, Balakrishnan D, Inaba-Inoue S, De Vries AH, Beis K, Marrink SJ, Heddle JG. CRAFTing Delivery of Membrane Proteins into Protocells using Nanodiscs.
  In: ACS Appl Mater Interfaces. 2023
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- Shah SN, Heddle JG, Evans DJ, Lomonossoff GP. Production of Metallic Alloy Nanowires and Particles Templated Using Tomato Mosaic Virus (ToMV).
  In: Nanomaterials (Basel). 2023
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- Saathoff M, Kosol S, Semmler T, Tedin K, Dimos N, Kupke J, Seidel M, Ghazisaeedi F, Jonske MC, Wolf SA, Kuropka B, Czyszczoń W, Ghilarov D, Grätz S, Heddle JG, Loll B, Süssmuth RD, Fulde M. Gene amplifications cause high-level resistance against albicidin in gram-negative bacteria.
  In: PLoS Biol. 2023
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- Zakaszewski D, Koziej L, Pankowski J, Malolan VV, Gämperli N, Heddle JG, Hilvert D, Azuma Y. Complementary charge-driven encapsulation of functional protein by engineered protein cages in cellulo.
  In: J Mater Chem B. 2023
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- Michalczyk E, Hommernick K, Behroz I, Kulike M, Pakosz-Stępień Z, Mazurek L, Seidel M, Kunert M, Santos K, von Moeller H, Loll B, Weston JB, Mainz A, Heddle JG, Süssmuth RD, Ghilarov D. Molecular mechanism of topoisomerase poisoning by the peptide antibiotic albicidin.
  In: Nat Catal. 2023
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2022
- Sharma M, Biela AP, Kowalczyk A, Borzęcka-Solarz K, Piette BMAG, Gaweł S, Bishop J, Kukura P, Benesch JLP, Imamura M, Scheuring S, Heddle JG. Shape-Morphing of an Artificial Protein Cage with Unusual Geometry Induced by a Single Amino Acid Change.
  In: ACS Nanosci Au. 2022
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- Sakai Y, Wilkens GD, Wolski K, Zapotoczny S, Heddle JG. Topogami: Topologically Linked DNA Origami.
  In: ACS Nanosci Au. 2022
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- Majsterkiewicz, A., Biela, A. P., Maity, S., Sharma, M.,2, Piette, B. M. A. G., Kowalczyk, A., Gaweł, S., Chakraborti, S., Roos, W. H., Heddle, J. G. (2022) An artificial protein cage with unusual geometry and regularly embedded gold nanoparticles.
  In: Nano Letters
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- Biela, A., Naskalska, A., Fatehi, F., Twarock, R., Heddle, J.G. (2022). Programmable Polymorphism of a Virus-Like Particle.
  In: Commun. Mater
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- Piette, B. M. A. G., Kowalczyk, A., Heddle, J.G., (2022). Characterisation of Near-miss Connectivity-Invariant Homogeneous Convex Polyhedral Cages.
  In: Proc. R. Soc.
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- Stupka, I., Azuma, Y., Biela, A.P., Imamura, M., Scheuring, S., Pyza, E., Woźnicka, O., Maskell, D.P. and Heddle, J.G.* (2022) Chemically induced protein cage assembly with programmable opening and cargo release.
  In: Sci. Adv.
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2021
- Naskalska, A., Borzęcka-Solarz, K., Różycki, J., Stupka, I., Bochenek, M., Pyza, E., Heddle, J. G.* (2021). Artificial Protein Cage Delivers Active Protein Cargos to the Cell Interior.
  In: Biomacromolecules
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- Kumar, M., Markiewicz-Mizera, J., Olmos, J. D. J., Wilk, P., Grudnik, P., Biela, A. P., Jemioła-Rzemińska, M., Górecki, A., Chakraborti, S., Heddle, J. G.* (2021). A single residue can modulate nanocage assembly in salt dependent ferritin.
  In: Nanoscale
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- Islam, M. S., Wilkens, G. D., Wolski, K., Zapotoczny, S., Heddle, J. G.* (2021). Chiral 3D DNA origami structures for ordered heterologous arrays.
  In: Nanoscale Adv.
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- Pakosz, Z., Lin, T. Y., Michalczyk, E., Nagano, S., Heddle, J. G.* (2021).Inhibitory compounds targeting Plasmodium falciparum gyrase B.,
  In: Antimicrob. Agents Chemother.
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- Ghilarov, D., Inaba-Inoue, S., Stepien, P., Qu, F., Michalczyk, E., Pakosz, Z., Nomura, N., Ogasawara, S., Walker, G. C., Rebuffat, S., Iwata, S., Heddle, J. G.*, Beis, K.* (2021). Molecular mechanism of SbmA, a promiscuous transporter exploited by antimicrobial peptides.
  In: Sci. Adv.
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- Mazurek, L., Ghilarov, D.*, Michalczyk, E., Pakosz, Z. Metelev, M., Czyszczon, W., Wawro, K., Behroz, I., Dubiley, S., Süssmuth, R., Heddle, J. G.* (2021) Pentapeptide repeat protein QnrB1 requires ATP hydrolysis to rejuvenate poisoned gyrase complexes.
  In: Nucl. Acids Res.
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2020
- Stupka I, Heddle JG. Artificial protein cages – inspiration, construction, and observation.
  In: Curr Opin Struct Biol. 2020
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- Majsterkiewicz K, Azuma Y, Heddle JG. Connectability of protein cages.
  In: Nanoscale Adv. 2020
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- Piette BMAG, Heddle JG. A Peptide-Nucleic Acid Replicator Origin for Life.
  In: Trends Ecol Evol. 2020
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- Chakraborti S, Lin TY, Glatt S, Heddle JG. Enzyme encapsulation by protein cages.
  In: RSC Adv. 2020
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- Chakraborti, S., Balakrishnan, D., Trotter, A.J., Gittens, W.H., Yang, A.W., Jolma, A., Paterson, J.R., Świątek, S., Plewka, J., Curtis, F.A., Bowers, L.Y., Pålsson, L.-O., Hughes, T. R., Taube, M., Kozak, M., Heddle, J. G.*, Sharples, G. J.*, (2020). A bacteriophage mimic of the bacterial nucleoid-associated protein
  In: Fis. Biochem. J.
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2019
- Chakraborti. S., Korpi, A., Kumar, M., Stępień, P., Kostiainen, M. A., Heddle, J.G.* (2019) A three-dimensional protein cage array capable of active enzyme capture and artificial chaperone activity
  In: Nano Letters
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- Malay, A. D.; Miyazaki, N.; Biela, A.; Chakraborti, S.; Majsterkiewicz, K.; Stupka, I.; Kaplan, C. S.; Kowalczyk, A.; Piette, B. M. A. G.; Hochberg, G. K. A.; Wu, D.; Wrobel, T. P.; Fineberg, A.; Kushwah, M. S.; Kelemen, M.; Vavpetič, P.; Pelicon, P.; Kukura, P.; Benesch, J. L. P.; Iwasaki, K.; Heddle, J. G. (2019) An ultra-stable gold-coordinated protein cage displaying reversible assembly
  In: Nature
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- Balakrishnan D, Wilkens GD, Heddle JG. Delivering DNA origami to cells.
  In: Nanomedicine (Lond). 2019
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2018
- Sakai, Y., Islam, M. S., Adamiak, M., Shiu, S.C.-C., Tanner, J. A., Heddle, J. G., (2018) DNA Aptamers for the Functionalisation of DNA Origami Nanostructures,
  In: Genes
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- Shiu, S.C.-C., Kinghorn, A.B., Sakai, Y., Cheung, Y-W., Heddle, J.G., Tanner, J.A. (2018) The Three S’s for Aptamer‐Mediated Control of DNA Nanostructure Dynamics: Shape, Self‐Complementarity, and Spatial Flexibility
  In: ChemBioChem 19,
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- Tang, M. S., Shiu, S. C-C., Godonoga, M., Cheung, Y-W., Liang, S., Dirkzwager, R. M., Kinghorn, A. B., Fraser, L. A., Heddle, J. G.*, Tanner, J. A.* (2018) An aptamer-enabled DNA nanobox for protein sensing
  In: Nanomedicine
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- Banwell, E. F., Piette, B., Taormina, A., Heddle, J. G. (2018) Reciprocal Nucleopeptides as the Ancestral Darwinian Self-Replicator
  In: Molec. Biol. Evol.
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2017
- Zaucha, J. & Heddle, J. G. (2017) Resurrecting the Dead (Molecules).
  In: Comp. Struc. Biotech. J.
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- Heddle, J. G. (2017) TRAPped Structures: Making Artificial Cages with a Ring Protein
  In: Advances in Bioinspired and Biomedical Materials
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- Heddle, J. G., Chakraborti, S., Iwasaki, K. (2017) Natural and Artificial Protein Cages: Design, Structure and Therapeutic Applications.
  In: Curr. Opin. Struc. Biol.
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2016
- Nagano, S.; Banwell, E. F.; Iwasaki, K.; Michalak, M.; Pałka, R.; Zhang, K. Y. J.; Voet, A. R. D.; Heddle, J. G. (2016) Understanding the Assembly of an Artificial Protein Nanotube
  In: Adv. Mater. Interfaces
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- Godonoga, M., Lin, T.-Y., Oshima, A., Sumitomo, K., Tang, M. S. L., Cheung, Y.-W., Kinghorn, A. B., Dirkzwager, R. M., Zhou, C., Kuzuya, A., Tanner, J. A., Heddle, J. G. (2016) A DNA aptamer recognising a malaria protein biomarker can function as part of a DNA origami assembly
  In: Sci. Rep
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- Shah, s., Khan, A., Espinosa, A., Garcia, M., Nuansing, W., Ungureanu, M., Heddle, J. G., Chuvilin, A., Wege, C., Bittner, A. (2016) Virus-Templated Near-Amorphous Iron Oxide Nanotubes.
  In: Langmuir
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2015
- Nagano, S., Seki, E., Lin, T-Y., Shirouzu, M., Yokoyama, S., Heddle, J. G. (2015) Investigating the roles of the C-terminal domain of Plasmodium falciparum GyrA.
  In: PLOS ONE
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- Lin, T.-Y., Nagano, S. & Gardiner Heddle, J. (2015). Functional Analyses of the Toxoplasma gondii DNA Gyrase Holoenzyme: A Janus Topoisomerase with Supercoiling and Decatenation Abilities.
  In: Sci. Rep.
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- Imamura, M., Uchihashi, T., Ando, T., Arisaka, F., Malay, A.D. and Heddle, J.G. (2015) Probing Structural Dynamics of an Artificial Protein Cage Using High-Speed Atomic Force Microscopy
  In: Nano Lett.
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- Shah, S. S., Shah, S. N. & Heddle, J. G. (2015) Polymer-Mediated Dual Mineralization of a Plant Virus: A Platinum Nanowire Encapsulated by Iron Oxide.
  In: Chem. Lett.
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2014
- Nagano, S., Lin, T., Reddy, J., Heddle, J. G. (2014) Unique Features of Apicoplast DNA Gyrases from Toxoplasma gondii and Plasmodium falciparum. BMC Bioinformatics. 15, 416 [Pubmed]
- Shah, S. & Heddle, J. G. (2014) Squaring up to DNA: pentapeptide repeat proteins and DNA mimicry. Appl. Microbiol. and Biot. 98, 9545-9560 [Springer]
- Shah, S. N., Shah, S. S., Ito, E., Heddle, J. G. (2014) Template-Free, Hollow and Porous Platinum Nanotube Derived from Tobamovirus and its Three-Dimensional Structure at the Nanoscale. RSC Advances 4, 39305-39311.[RSC]
- Curtis, F. A. et al. (2014) Phage Orf family recombinases: conservation of activities and involvement of the central channel in DNA binding. PLOS ONE (2014). [PLOS]
- Yamazaki, T., Heddle, J.G. Kuzuya, A. and Komiyama, M. (2014) Orthogonal Enzyme Arrays on a DNA Origami Scaffold Bearing Size-Tunable Wells. Nanoscale 6, 9122-9126 [RSC]
2013 – 2002
- Matsubara, K., Malay, A. D., Curtis, F. A. Sharples, G. J., Heddle, J. G. (2013). Structural and functional characterization of the Redβ recombinase from bacteriophage λ. PLOS ONE 8, e78869 [PLOS]
- Tsukamoto, R., Godonoga, M., Matsuyama, R., Igarashi, M., Heddle, J.G., Samukawa, S. and Yamashita, I. (2013) The effect of PEGylation on Controllably-Spaced Adsorption of Ferritin Molecules. Langmuir 29, 12737-12743 [ACS]
- Trindade, L. S., Aigaki, T., Peixoto, A. A., Balduino, A., da Cruz, I. B. M., nica & Heddle, J. G. (2013). A novel classification system for aging theories. Frontiers Genet. 4. [Froniters ]
- Voet, A., Banwell, E. F., Sahu, K. K., Heddle, J. G. & Zhang, K. Y. (2013). Protein Interface Pharmacophore Mapping Tools for Small Molecule Protein:Protein Interaction Inhibitor Discovery. Curr. Top. Med. Chem. 13, 989-1001 [Pubmed]
- Heddle, J. G., (2013). Gold Nanoparticle-Biological Molecule Interactions and Catalysis. Catalysts 3. 683-708[Full Text]
- Malay, A. D., Heddle, J. G*., Tomita, S., Iwasaki, K., Miyazaki, N., Sumitomo, K., Yanagi, H., Yamashita, I. & Uraoka, Y. (2012). Gold Nanoparticle-Induced Formation of Artificial Protein Capsids. Nano Lett. 12, 2056-2059 [PDF]
- Heddle, J. G.* & Tame, J. R. H. (2012). Protein nanotubes, channels and cages. In Amino Acids, Peptides and Proteins (Farkas, E. & Ryadnov, M., eds.), Vol. 37, pp. 151-189. The Royal Society of Chemistry, Cambridge [RSC]
- Trindade, L., Balduino, A., Aigaki, T. and Heddle, J. (2012) Senemorphism: a novel perspective on aging patterns and its implication for diet-related biology. Biogerontology, 13, 457-466. [PUBMED
- Malay, A. D., Watanabe, M., Heddle, J. G*. & Tame, J. R. H. (2011). Crystal structure of unliganded TRAP: implications for dynamic allostery. Biochem. J. 434, 429-434. [PUBMED]
- Watanabe, M., Heddle, J. G#., Kikuchi, K., Unzai, S., Akashi, S., Park, S. Y. & Tame, J. R. (2009). The nature of the TRAP-Anti-TRAP complex. Proc. Natl. Acad. Sci. USA 106, 2176-2181. [PUBMED]
- Miranda, F. F., Iwasaki, K., Akashi, S., Sumitomo, K., Kobayashi, M., Yamashita, I., Tame, J. R. H. & Heddle, J. G. (2009). A Self-Assembled Protein Nanotube with High Aspect Ratio. Small 5, 2077-2084. [PUBMED]
- Akashi, S., Watanabe, M., Heddle, J. G., Unzai, S., Park, S. Y. & Tame, J. R. (2009). RNA and Protein Complexes of trp RNA-Binding Attenuation Protein Characterized by Mass Spectrometry. Anal. Chem. 81, 2218-2226. [PUBMED]
- Watanabe, M., Mishima, Y., Yamashita, I., Park, S.-Y., Tame, J. R. H. & Heddle, J. G. (2008). Intersubunit linker length as a modifier of protein stability: Crystal structures and thermostability of mutant TRAP. Protein Sci. 17, 518-526. [WILEY]
- Heddle, J. G. (2008). Protein cages,rings and tubes:useful components of future nanodevices? Nanotechnology, Science and Applications 1, 67-78. [NCBI]
- Yoshizawa, K., Mishima, Y., Park, S. Y., Heddle, J. G., Tame, J. R., Iwahori, K., Kobayashi, M. & Yamashita, I. (2007). Effect of N-terminal residues on the structural stability of recombinant horse L-chain apoferritin in an acidic environment. J. Biochem. (Tokyo) 142, 707-713. [PUBMED]
- Heddle, J. G*., Okajima, T., Scott, D. J., Akashi, S., Park, S. Y. & Tame, J. R. (2007). Dynamic allostery in the ring protein TRAP. J. Mol. Biol. 371, 154-167. [ScienceDirect]
- Heddle, J. G*., Fujiwara, I., Yamadaki, H., Yoshii, S., Nishio, K., Addy, C., Yamashita, I. & Tame, J. R. (2007). Using the ring-shaped protein TRAP to capture and confine gold nanodots on a surface. Small 3, 1950-6. [PUBMED]
- Addy, C., Ohara, M., Kawai, F., Kidera, A., Ikeguchi, M., Fuchigami, S., Osawa, M., Shimada, I., Park, S. Y., Tame, J. R. & Heddle, J. G. (2007). Nickel binding to NikA: an additional binding site reconciles spectroscopy, calorimetry and crystallography. Acta. Crystallogr. D. Bio.l Crystallogr. 63, 221-229. [PUBMED]
- Heddle, J. G., Yokoyama, T., Yamashita, I., Park, S. Y. & Tame, J. R. (2006). Rounding up: Engineering 12-membered rings from the cyclic 11-mer TRAP. Structure 14, 925-33. [ScienceDirect]
- Rajesh, S., Heddle, J. G., Kurashima-Ito, K., Nietlispach, D., Shirakawa, M., Tame, J. R. & Ito, Y. (2005). Backbone 1H, 13C, and 15N assignments of a 56 kDa E. coli nickel binding protein NikA. J, Biomol. NMR 32, 177. [PUBMED]
- Otto, B. R., Sijbrandi, R., Luirink, J., Oudega, B., Heddle, J. G., Mizutani, K., Park, S. Y. & Tame, J. R. (2005). Crystal structure of hemoglobin protease, a heme binding autotransporter protein from pathogenic Escherichia coli. J. Biol. Chem. 280, 17339-17345. [JBC]
- Heddle, J. G., Mitelheiser, S., Maxwell, A. & Thomson, N. H. (2004). Nucleotide binding to DNA gyrase causes loss of DNA wrap. J. Mol. Biol. 337, 597-610. [PUBMED]
- Heddle, J., Scott, D. J., Unzai, S., Park, S. Y. & Tame, J. R. (2003). Crystal structures of the liganded and unliganded nickel-binding protein NikA from Escherichia coli. J. Biol. Chem. 278, 50322-50329. [PUBMED]
- Strumberg, D., Nitiss, J. L., Dong, J., Walker, J., Nicklaus, M. C., Kohn, K. W., Heddle, J. G., Maxwell, A., Seeber, S. & Pommier, Y. (2002). Importance of the fourth alpha-helix within the CAP homology domain of type II topoisomerase for DNA cleavage site recognition and quinolone action. Antimicrob. Agents Chemother. 46, 2735-2746. [PUBMED]
- Heddle, J. & Maxwell, A. (2002). Quinolone-binding pocket of DNA gyrase: role of GyrB. Antimicrob Agents Chemother 46, 1805-1815. [PUBMED]
- Zamble, D. B., Miller, D. A., Heddle, J. G., Maxwell, A., Walsh, C. T. & Hollfelder, F. (2001). In vitro characterization of DNA gyrase inhibition by microcin B17 analogs with altered bisheterocyclic sites. Proc. Natl. Acad. Sci. USA 98, 7712-7717. [PNAS]
- Heddle, J. G., Lu, T., Zhao, X., Drlica, K. & Maxwell, A. (2001). gyrB-225, a mutation of DNA gyrase that compensates for topoisomerase I deficiency: investigation of its low activity and quinolone hypersensitivity. J. Mol. Biol. 309, 1219-1231. [ScienceDirect]
- Heddle, J. G., Blance, S. J., Zamble, D. B., Hollfelder, F., Miller, D. A., Wentzell, L. M., Walsh, C. T. & Maxwell, A. (2001). The antibiotic microcin B17 is a DNA gyrase poison: characterisation of the mode of inhibition. J. Mol. Biol. 307, 1223-1234. [PUBMED]
- Heddle, J. G., Barnard, F. M., Wentzell, L. M. & Maxwell, A. (2000). The interaction of drugs with DNA gyrase: a model for the molecular basis of quinolone action. Nucleosides Nucleotides Nucleic Acids 19, 1249-1264. [PUBMED]