Professor Per Bullough

All publications

Journal articles

• Lanzoni-Mangutchi P, Banerji O, Wilson J, Barwinska-Sendra A, Kirk JA, Vaz F, O’Beirne S, Baslé A, El Omari K, Wagner A , Fairweather NF et al (2022) Structure and assembly of the S-layer in C. difficile. Nature Communications, 13(1). View this article in WRRO
• Salamaga B, Kong L, Pasquina-Lemonche L, Lafage L, von und zur Muhlen M, Gibson JF, Grybchuk D, Tooke AK, Panchal V, Culp EJ , Tatham E et al (2021) Demonstration of the role of cell wall homeostasis in Staphylococcus aureus growth and the action of bactericidal antibiotics. Proceedings of the National Academy of Sciences, 118(44), e2106022118-e2106022118.
• Janganan TK, Mullin N, Dafis-Sagarmendi A, Brunt J, Tzokov SB, Stringer S, Moir A, Chaudhuri RR, Fagan RP, Hobbs JK & Bullough PA (2020) Architecture and Self-Assembly of Clostridium sporogenes and Clostridium botulinum Spore Surfaces Illustrate a General Protective Strategy across Spore Formers. mSphere, 5(-), ---. View this article in WRRO
• Pasquina-Lemonche L, Burns J, Turner RD, Kumar S, Tank R, Mullin N, Wilson JS, Chakrabarti B, Bullough PA, Foster SJ & Hobbs JK (2020) The architecture of the Gram-positive bacterial cell wall. Nature, 582(7811), 294-297. View this article in WRRO
• Wilson JS, Churchill-Angus AM, Davies SP, Sedelnikova SE, Tzokov SB, Rafferty JB, Bullough PA, Bisson C & Baker PJ (2019) Identification and structural analysis of the tripartite α-pore forming toxin of Aeromonas hydrophila. Nature Communications, 10(1), ---. View this article in WRRO
• Ji S, Dix SR, Aziz AA, Sedelnikova SE, Baker PJ, Rafferty JB, Bullough PA, Tzokov SB, Agirre J, Li F-L & Rice DW (2019) The molecular basis of endolytic activity of a multidomain alginate lyase from Defluviitalea phaphyphila, a representative of a new lyase family, PL39. Journal of Biological Chemistry, 294(48), 18077-18091.
• Hill CJ, Fleming JR, Mousavinejad M, Nicholson R, Tzokov SB, Bullough PA, Bogomolovas J, Morgan MR, Mayans O & Murray P (2019) Self‐Assembling Proteins as High‐Performance Substrates for Embryonic Stem Cell Self‐Renewal. Advanced Materials, 31(17), 1807521-1807521.
• Dix SR, Owen HJ, Sun R, Ahmad A, Shastri S, Spiewak HL, Mosby DJ, Harris MJ, Batters SL, Brooker TA , Tzokov SB et al (2018) Structural insights into the function of type VI secretion system TssA subunits.. Nature Communications, 9(-), ---. View this article in WRRO
• Terry C, Jiang S, Radford DS, Qiang W, Tzokov S, Moir A & Bullough PA (2017) Molecular tiling on the surface of a bacterial spore – the exosporium of the Bacillus anthracis/cereus/thuringiensis group. Molecular Microbiology, 104(4), 539-552. View this article in WRRO
• Janganan TK, Mullin N, Tzokov SB, Stringer S, Fagan RP, Hobbs JK, Moir A & Bullough PA (2016) Characterization of the spore surface and exosporium proteins of Clostridium sporogenes; implications for Clostridium botulinum group I strains. Food Microbiology, 59, 205-212. View this article in WRRO
• Ma C, Hao Z, Huysmans G, Lesiuk A, Bullough P, Wang Y, Bartlam M, Phillips SE, Young JD, Goldman A , Baldwin SA et al (2015) A Versatile Strategy for Production of Membrane Proteins with Diverse Topologies: Application to Investigation of Bacterial Homologues of Human Divalent Metal Ion and Nucleoside Transporters. PLOS ONE, 10(11), e0143010-e0143010. View this article in WRRO
• Jiang S, Wan Q, Krajcikova D, Tang J, Tzokov SB, Barak I & Bullough PA (2015) Diverse supramolecular structures formed by self-assembling proteins of the B acillus subtilis spore coat. Molecular Microbiology, 97(2), 347-359. View this article in WRRO
• Adams NBP, Marklew CJ, Qian P, Brindley AA, Davison PA, Bullough PA & Hunter CN (2014) Structural and functional consequences of removing the N-terminal domain from the magnesium chelatase ChlH subunit of Thermosynechococcus elongatus. Biochemical Journal, 464(3), 315-322. View this article in WRRO
• Yamashita M, Shepherd M, Booth WI, Xie H, Postis V, Nyathi Y, Tzokov SB, Poole RK, Baldwin SA & Bullough PA (2014) Structure and function of the bacterial heterodimeric ABC transporter CydDC: stimulation of ATPase activity by thiol and heme compounds.. J Biol Chem, 289(33), 23177-23188. View this article in WRRO
• Qian P, Papiz MZ, Jackson PJ, Brindley AA, Ng IW, Olsen JD, Dickman MJ, Bullough PA & Hunter CN (2013) Three-dimensional structure of the Rhodobacter sphaeroides RC-LH1-PufX complex: dimerization and quinone channels promoted by PufX.. Biochemistry, 52(43), 7575-7585.
• Huysmans GHM, Chan N, Baldwin JM, Postis VLG, Tzokov SB, Deacon SE, Yao SYM, Young JD, McPherson MJ, Bullough PA & Baldwin SA (2012) A urea channel from Bacillus cereus reveals a novel hexameric structure.. Biochem J, 445(2), 157-166.
• Qian P, Marklew CJ, Viney J, Davison PA, Brindley AA, Söderberg C, Al-Karadaghi S, Bullough PA, Grossmann JG & Hunter CN (2012) Structure of the cyanobacterial Magnesium Chelatase H subunit determined by single particle reconstruction and small-angle X-ray scattering.. J Biol Chem, 287(7), 4946-4956.
• Glover CAP, Postis VLG, Charalambous K, Tzokov SB, Booth WI, Deacon SE, Wallace BA, Baldwin SA & Bullough PA (2011) AcrB contamination in 2-D crystallization of membrane proteins: lessons from a sodium channel and a putative monovalent cation/proton antiporter.. J Struct Biol, 176(3), 419-424.
• Kailas L, Terry C, Abbott N, Taylor R, Mullin N, Tzokov SB, Todd SJ, Wallace BA, Hobbs JK, Moir A & Bullough PA (2011) Surface architecture of endospores of the Bacillus cereus/anthracis/thuringiensis family at the subnanometer scale.. Proc Natl Acad Sci U S A, 108(38), 16014-16019.
• Terry C, Shepherd A, Radford DS, Moir A & Bullough PA (2011) YwdL in Bacillus cereus: its role in germination and exosporium structure.. PLoS One, 6(8), e23801. View this article in WRRO
• Glover CAP, Postis VLG, Charalambous K, Tzokov SB, Booth WI, Deacon SE, Wallace BA, Baldwin SA & Bullough PA (2011) AcrB contamination in 2-D crystallization of membrane proteins: Lessons from a sodium channel and a putative monovalent cation/proton antiporter. Journal of Structural Biology, 176(3), 419-424.
• Charalambous K, O'Reilly AO, Bullough PA & Wallace BA (2009) Thermal and chemical unfolding and refolding of a eukaryotic sodium channel.. Biochim Biophys Acta, 1788(6), 1279-1286. View this article in WRRO
• Ball DA, Taylor R, Todd SJ, Redmond C, Couture-Tosi E, Sylvestre P, Moir A & Bullough PA (2008) Structure of the exosporium and sublayers of spores of the Bacillus cereus family revealed by electron crystallography.. Mol Microbiol, 68(4), 947-958.
• Baboolal TG, Conroy MJ, Gill K, Ridley H, Visudtiphole V, Bullough PA & Lakey JH (2008) Colicin N binds to the periphery of its receptor and translocator, outer membrane protein F.. Structure, 16(3), 371-379.
• Qian P, Bullough PA & Hunter CN (2008) Three-dimensional reconstruction of a membrane-bending complex: the RC-LH1-PufX core dimer of Rhodobacter sphaeroides.. J Biol Chem, 283(20), 14002-14011.
• Hunt S, Moir AJG, Tzokov S, Bullough PA, Artymiuk PJ & Green J (2008) The formation and structure of Escherichia coli K-12 haemolysin E pores.. Microbiology, 154(Pt 2), 633-642.
• Qian P, Bullough P & Hunter N (2007) Single particle analysis of the dimeric RC-LH1-PufX complex from Rhodobacter sphaeroides. PHOTOSYNTH RES, 91(2-3), 171-171.
• Conroy MJ, Durand A, Lupo D, Li X-D, Bullough PA, Winkler FK & Merrick M (2007) The crystal structure of the Escherichia coli AmtB-GlnK complex reveals how GlnK regulates the ammonia channel.. Proc Natl Acad Sci U S A, 104(4), 1213-1218.
• Tzokov SB, Wyborn NR, Stillman TJ, Jamieson S, Czudnochowski N, Artymiuk PJ, Green J & Bullough PA (2006) Structure of the hemolysin E (HlyE, ClyA, and SheA) channel in its membrane-bound form.. J Biol Chem, 281(32), 23042-23049.
• Merrick M, Javelle A, Durand A, Severi E, Thornton J, Avent ND, Conroy MJ & Bullough PA (2006) The Escherichia coli AmtB protein as a model system for understanding ammonium transport by Amt and Rh proteins.. Transfus Clin Biol, 13(1-2), 97-102.
• Conroy MJ, Bullough PA, Merrick M & Avent ND (2005) Modelling the human rhesus proteins: implications for structure and function.. Br J Haematol, 131(4), 543-551.
• Stillman TJ, Upadhyay M, Norte VA, Sedelnikova SE, Carradus M, Tzokov S, Bullough PA, Shearman CA, Gasson MJ, Williams CH , Artymiuk PJ et al (2005) The crystal structures of Lactococcus lactis MG1363 Dps proteins reveal the presence of an N-terminal helix that is required for DNA binding.. Mol Microbiol, 57(4), 1101-1112.
• Jelinska C, Conroy MJ, Craven CJ, Hounslow AM, Bullough PA, Waltho JP, Taylor GL & White MF (2005) Obligate heterodimerization of the archaeal Alba2 protein with Alba1 provides a mechanism for control of DNA packaging.. Structure, 13(7), 963-971.
• Qian P, Hunter CN & Bullough PA (2005) The 8.5A projection structure of the core RC-LH1-PufX dimer of Rhodobacter sphaeroides.. J Mol Biol, 349(5), 948-960.
• Conroy MJ, Jamieson SJ, Blakey D, Kaufmann T, Engel A, Fotiadis D, Merrick M & Bullough PA (2004) Electron and atomic force microscopy of the trimeric ammonium transporter AmtB.. EMBO Rep, 5(12), 1153-1158.
• Bahatyrova S, Frese RN, Siebert CA, Olsen JD, Van Der Werf KO, Van Grondelle R, Niederman RA, Bullough PA, Otto C & Hunter CN (2004) The native architecture of a photosynthetic membrane.. Nature, 430(7003), 1058-1062. View this article in WRRO
• Wyborn NR, Clark A, Roberts RE, Jamieson SJ, Tzokov S, Bullough PA, Stillman TJ, Artymiuk PJ, Galen JE, Zhao L , Levine MM et al (2004) Properties of haemolysin E (HlyE) from a pathogenic Escherichia coli avian isolate and studies of HlyE export.. Microbiology, 150(Pt 5), 1495-1505.
• Siebert CA, Qian P, Fotiadis D, Engel A, Hunter CN & Bullough PA (2004) Molecular architecture of photosynthetic membranes in Rhodobacter sphaeroides: the role of PufX.. EMBO J, 23(4), 690-700.
• Fotiadis D, Qian P, Philippsen A, Bullough PA, Engel A & Hunter CN (2004) Structural analysis of the reaction center light-harvesting complex I photosynthetic core complex of Rhodospirillum rubrum using atomic force microscopy.. J Biol Chem, 279(3), 2063-2068.
• Bullough PA (2004) Conformational flexibility in assembly of photosynthetic membrane protein complexes in vivo. Microscopy and Microanalysis, 10(SUPPL. 2), 1496-1497.
• Olsen JD, Robert B, Siebert CA, Bullough PA & Hunter CN (2003) Role of the C-terminal extrinsic region of the alpha polypeptide of the light-harvesting 2 complex of Rhodobacter sphaeroides: a domain swap study.. Biochemistry, 42(51), 15114-15123.
• Qian P, Addlesee HA, Ruban AV, Wang P, Bullough PA & Hunter CN (2003) A reaction center-light-harvesting 1 complex (RC-LH1) from a Rhodospirillum rubrum mutant with altered esterifying pigments: characterization by optical spectroscopy and cryo-electron microscopy.. J Biol Chem, 278(26), 23678-23685.
• Reid JD, Siebert CA, Bullough PA & Hunter CN (2003) The ATPase activity of the ChlI subunit of magnesium chelatase and formation of a heptameric AAA+ ring.. Biochemistry, 42(22), 6912-6920.
• Jamieson SJ, Wang P, Qian P, Kirkland JY, Conroy MJ, Hunter CN & Bullough PA (2002) Projection structure of the photosynthetic reaction centre-antenna complex of Rhodospirillum rubrum at 8.5 A resolution.. EMBO J, 21(15), 3927-3935.
• Ruzheinikov SN, Burke J, Sedelnikova S, Baker PJ, Taylor R, Bullough PA, Muir NM, Gore MG & Rice DW (2001) Glycerol dehydrogenase. structure, specificity, and mechanism of a family III polyol dehydrogenase.. Structure, 9(9), 789-802.
• Prince SM, Feron C, Janssens D, Lobet Y, Achtman M, Kusecek B, Bullough PA & Derrick JP (2001) Expression, refolding and crystallization of the OpcA invasin from Neisseria meningitidis.. Acta Crystallogr D Biol Crystallogr, 57(Pt 8), 1164-1166.
• Yin CC, Aldema-Ramos ML, Borges-Walmsley MI, Taylor RW, Walmsley AR, Levy SB & Bullough PA (2000) The quarternary molecular architecture of TetA, a secondary tetracycline transporter from Escherichia coli.. Mol Microbiol, 38(3), 482-492.
• Wallace AJ, Stillman TJ, Atkins A, Jamieson SJ, Bullough PA, Green J & Artymiuk PJ (2000) E. coli hemolysin E (HlyE, ClyA, SheA): X-ray crystal structure of the toxin and observation of membrane pores by electron microscopy.. Cell, 100(2), 265-276.
• Collins R, Achtman M, Ford R, Bullough P & Derrick J (1999) Projection structure of reconstituted Opc outer membrane protein from Neisseria meningitidis. MOL MICROBIOL, 32(1), 217-219.
• Bullough PA & Henderson R (1999) The projection structure of the low temperature K intermediate of the bacteriorhodopsin photocycle determined by electron diffraction.. J Mol Biol, 286(5), 1663-1671.
• Subramaniam S, Lindahl M, Bullough PA, Faruqi AR, Tittor J, Oesterhelt D, Brown L, Lanyi J & Henderson R (1999) Protein Conformational Changes in the Bacteriorhodopsin Photocycle. Journal of Molecular Biology, 287, 145-161.
• Walz T, Jamieson SJ, Bowers CM, Bullough PA & Hunter CN (1998) Projection structures of three photosynthetic complexes from Rhodobacter sphaeroides: LH2 at 6 A, LH1 and RC-LH1 at 25 A.. J Mol Biol, 282(4), 833-845.
• Henderson R, Bullough P, Lindahl M & Subramaniam S (1997) Structural changes underlying proton pumping by Bacteriorhodopsin. FASEB J, 11(9), A992-A992.
• Karrasch S, Bullough PA & Ghosh R (1995) The 8.5 A projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits.. EMBO J, 14(4), 631-638.
• Skehel JJ, Bizebard T, Bullough PA, Hughson FM, Knossow M, Steinhauer DA, Wharton SA & Wiley DC (1995) Membrane fusion by influenza hemagglutinin.. Cold Spring Harb Symp Quant Biol, 60, 573-580.
• Bullough PA, Hughson FM, Treharne AC, Ruigrok RW, Skehel JJ & Wiley DC (1994) Crystals of a fragment of influenza haemagglutinin in the low pH induced conformation.. J Mol Biol, 236(4), 1262-1265.
• Bullough PA, Hughson FM, Skehel JJ & Wiley DC (1994) Structure of influenza haemagglutinin at the pH of membrane fusion.. Nature, 371(6492), 37-43.
• Bullough PA & Tulloch PA (1991) Spot-scan imaging of microcrystals of an influenza neuraminidase-antibody fragment complex.. Ultramicroscopy, 35(2), 131-143.
• Bullough PA & Tulloch PA (1990) High-resolution spot-scan electron microscopy of microcrystals of an alpha-helical coiled-coil protein.. J Mol Biol, 215(1), 161-173.
• Bullough PA & Henderson R (1990) Phase accuracy in high-resolution electron microscopy of trigonal and orthorhombic purple membrane.. Biophys J, 58(3), 705-711.
• Bullough PA (1990) Imaging of protein molecules--towards atomic resolution.. Electron Microsc Rev, 3(2), 249-267.
• BULLOUGH P & HENDERSON R (1987) USE OF SPOT-SCAN PROCEDURE FOR RECORDING LOW-DOSE MICROGRAPHS OF BEAM-SENSITIVE SPECIMENS. ULTRAMICROSCOPY, 21(3), 223-229.
• Al-Otaibi N, Baatsen P, Bhella D, Brescia R, Bullough P, Daum B, de Bruin R, Frank R, Kühlbrandt W, López-Iglesias C , McLaren M et al () Tomographic analysis, CLEM: general discussion. Faraday Discussions, 240, 142-151.
• Bakker SE, Bhella D, Brescia R, Bullough P, Clare DK, Daum B, Frank RAW, Gold VAM, Jackson Hirst I, Kühlbrandt W , Lu P et al () Pushing the limits in single particle cryo-EM: general discussion. Faraday Discussions.
• Al-Otaibi N, Aminian J. A, Anane RF, Baatsen P, Bakker SE, Bergeron J, Bharadwaj A, Bhella D, Braun T, Brescia R , Bullough P et al () Sample preparation in single particle cryo-EM: general discussion. Faraday Discussions.
• Bakker SE, Bergeron J, Bharadwaj A, Bhella D, Bullough P, Chau P-L, Frank RAW, Jakobi AJ, Joseph AP, Kühlbrandt W , Lahiri I et al () Map/model validation and machine learning in EM: general discussion. Faraday Discussions.
• Tank RKG, Lund VA, Kumar S, Turner RD, Lafage L, Pasquina Lemonche L, Bullough PA, Cadby A, Foster SJ & Hobbs JK () Correlative Super-Resolution Optical and Atomic Force Microscopy Reveals Relationships Between Bacterial Cell Wall Architecture and Synthesis in Bacillus subtilis. ACS Nano.

Chapters

• Shewring JR, Hodgson L, Bryant HL, Bullough PA, Weinstein JA & Verkade P (2021) Refining a correlative light electron microscopy workflow using luminescent metal complexes, Methods in Cell Biology (pp. 69-87). Elsevier
• Bullough P (2013) Electron Diffraction, Encyclopedia of Biophysics (pp. 581-586). Springer Berlin Heidelberg
• Bullough PA, Qian P & Hunter CN (2009) Reaction Center-Light-Harvesting Core Complexes of Purple Bacteria, The Purple Phototrophic Bacteria (pp. 155-179). Springer Netherlands
• Karrasch S, Bullough PA & Ghosh R (1995) 8.5 Å Projection Map of the Light-Harvesting Complex I from Rhodospirillum Rubrum Reveals a Ring Composed of 16 Subunits, Photosynthesis: from Light to Biosphere (pp. 81-84). Springer Netherlands

Conference proceedings papers

• Baboolal TG, Conroy MJ, Gill K, Bullough P & Lakey JH (2005) The colicin N- OmpF translocation complex. BIOPHYSICAL JOURNAL, Vol. 88(1) (pp 50A-51A)
• Bullough PA, Jamieson SJ, Walz T, Hunter CN, Bowers CM, Karrasch S, Ghosh R, Henderson R & Subramaniam S (1999) Energy production in biological systems probed by electron crystallography. ELECTRON MICROSCOPY AND ANALYSIS 1999(161) (pp 127-132)
• Bullough PA (1996) Conformational changes in influenza haemagglutinin at the pH of membrane fusion. OPTIONS FOR THE CONTROL OF INFLUENZA III, Vol. 1123 (pp 307-314)
• Karrasch S, Bullough PA & Ghosh R (1995) 8.5 angstrom projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits. PHOTOSYNTHESIS: FROM LIGHT TO BIOSPHERE, VOL I (pp 81-84)
• SKEHEL JJ, STEINHAUER D, WHARTON SA, BULLOUGH PA, HUGHSON FM, WATOWICH SJ & WILEY DC (1994) RECEPTOR BINDING AND MEMBRANE FUSION BY INFLUENZA HEMAGGLUTININ. CELLULAR RECEPTORS FOR ANIMAL VIRUSES (pp 187-193)

Datasets

• Lemonche LP, Burns J, Turner R, Kumar S, Tank R, Mullin N, Wilson J, Chakrabarti B, Bullough P, Foster S & Hobbs J The architecture of the Gram-positive bacterial cell wall.

Preprints

• Stevenson SR, Tzokov SB, Lahiri I, Ayscough KR & Bullough PA (2024) CryoEM Reconstruction of Yeast ADP-Actin Filament at 2.5 Å resolution. A comparison with mammalian and avian F-actin, Cold Spring Harbor Laboratory.
• Wilson JS, Fortier L-C, Fagan RP & Bullough PA (2023) Molecular mechanism of bacteriophage tail contraction- structure of an S-layer-penetrating bacteriophage.
• Banerji O, Lanzoni-Mangutchi P, Vaz F, Barwinska-Sendra A, Wilson J, Kirk J, O'Beirne S, Basle A, Omari KE, Wagner A , Fairweather N et al () Structure and assembly of the S-layer determine virulence in C. difficile. View this article in WRRO
• Janganan TK, Mullin N, Dafis-Sagarmendi A, Brunt J, Tzokov SB, Stringer S, Moir A, Chaudhuri R, Fagan RP, Hobbs JK & Bullough PA () Architecture and self-assembly of theClostridium sporogenes/botulinumspore surface illustrate a general protective strategy across spore formers.
• Mohasin M, Balbirnie-Cumming K, Fisk E, Prestwich EC, Russell CD, Marshall J, Pridans C, Allen SP, Shaw PJ, De Vos KJ , Hill CJ et al () Mitochondrial fission is increased in macrophages during mROS production in response to S. pneumoniae, Cold Spring Harbor Laboratory.