The Microbial Toxin Microcin B17: Prospects for the Development of New Antibacterial Agents

Journal of Molecular Biology - Tập 431 - Trang 3400-3426 - 2019
Frederic Collin1, Anthony Maxwell1
1Department Biological Chemistry, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, UK

Tài liệu tham khảo

Bax, 2015, Antibiotics: the changing regulatory and pharmaceutical industry paradigm, J. Antimicrob. Chemother., 70, 1281, 10.1093/jac/dku572 O'Brien, 2015, Meeting the societal need for new antibiotics: the challenges for the pharmaceutical industry, Br. J. Clin. Pharmacol., 79, 168, 10.1111/bcp.12401 Payne, 2007, Drugs for bad bugs: confronting the challenges of antibacterial discovery, Nat. Rev. Drug Discov., 6, 29, 10.1038/nrd2201 Tommasi, 2015, ESKAPEing the labyrinth of antibacterial discovery, Nat. Rev. Drug Discov., 14, 529, 10.1038/nrd4572 Coates, 2011, Novel classes of antibiotics or more of the same?, Br. J. Pharmacol., 163, 184, 10.1111/j.1476-5381.2011.01250.x Walsh, 2016 Aldred, 2014, Mechanism of quinolone action and resistance, Biochemistry., 53, 1565, 10.1021/bi5000564 Bush, 2015, DNA topoisomerases, EcoSal Plus, 6, 10.1128/ecosalplus.ESP-0010-2014 Duquesne, 2007, Microcins, gene-encoded antibacterial peptides from enterobacteria, Nat. Prod. Rep., 24, 708, 10.1039/b516237h Arnison, 2013, Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature, Nat. Prod. Rep., 30, 108, 10.1039/C2NP20085F Parks, 2007, The action of the bacterial toxin, microcin B17, on DNA gyrase, Biochimie., 89, 500, 10.1016/j.biochi.2006.12.005 Asensio Davagnino, 1986, The DNA replication inhibitor microcin B17 is a forty-three-amino-acid protein containing sixty percent glycine, Proteins Struct. Funct. Bioinforma., 1, 230, 10.1002/prot.340010305 Bayer, 1993, Posttranslational backbone modifications in the ribosomal biosynthesis of the glycine-rich antibiotic microcin B17, Angew. Chemie Int. Ed. English., 32, 1336, 10.1002/anie.199313361 Yorgey, 1994, Posttranslational modifications in microcin B17 define an additional class of DNA gyrase inhibitor, Proc. Natl. Acad. Sci. U. S. A., 91, 4519, 10.1073/pnas.91.10.4519 Yorgey, 1993, The maturation pathway of microcin B17, a peptide inhibitor of DNA gyrase, Mol. Microbiol., 9, 897, 10.1111/j.1365-2958.1993.tb01747.x Kelleher, 1999, Posttranslational heterocyclization of cysteine and serine residues in the antibiotic microcin B17: distributivity and directionality, Biochemistry., 38, 15623, 10.1021/bi9913698 D. Ghilarov, M. Serebryakova, I. Shkundina, K. Severinov, A major portion of DNA gyrase inhibitor microcin B17 undergoes an N,O-peptidyl shift during synthesis., J. Biol. Chem. 286 (2011) 26308–18. https://doi.org/10.1074/jbc.M111.241315. M. Herrero, F. Moreno, Microcin B17 blocks DNA replication and induces the SOS system in Escherichia coli., J. Gen. Microbiol. 132 (1986) 393–402. doi:https://doi.org/10.1099/00221287-132-2-393. J.L. Vizan, C. Hernandez-Chico, I. del Castillo, F. Moreno, The peptide antibiotic microcin B17 induces double-strand cleavage of DNA mediated by E. coli DNA gyrase, Embo J. 10 (1991) 467–476. Zamble, 2001, In vitro characterization of DNA gyrase inhibition by microcin B17 analogs with altered bisheterocyclic sites, Proc. Natl. Acad. Sci. U. S. A., 98, 7712, 10.1073/pnas.141225698 O.A. Pierrat, A. Maxwell, The action of the bacterial toxin microcin B17. Insight into the cleavage-religation reaction of DNA gyrase., J. Biol. Chem. 278 (2003) 35016–23. https://doi.org/10.1074/jbc.M304516200. Heddle, 2001, The antibiotic microcin B17 is a DNA gyrase poison: characterisation of the mode of inhibition, J. Mol. Biol., 307, 1223, 10.1006/jmbi.2001.4562 Costenaro, 2007, Modular structure of the full-length DNA gyrase B subunit revealed by small-angle x-ray scattering, Structure., 15, 329, 10.1016/j.str.2007.01.013 Williams, 1999, Probing the two-gate mechanism of DNA gyrase using cysteine cross-linking, Biochemistry., 38, 13502, 10.1021/bi9912488 Cove, 1997, DNA gyrase can cleave short DNA fragments in the presence of quinolone drugs, Nucleic Acids Res., 25, 2716, 10.1093/nar/25.14.2716 Pierrat, 2005, Evidence for the role of DNA strand passage in the mechanism of action of microcin B17 on DNA gyrase, Biochemistry., 44, 4204, 10.1021/bi0478751 Metelev, 2013, Structure of microcin B-like compounds produced by Pseudomonas syringae and species specificity of their antibacterial action, J. Bacteriol., 195, 4129, 10.1128/JB.00665-13 Cox, 2015, The genomic landscape of ribosomal peptides containing thiazole and oxazole heterocycles, BMC Genomics, 16, 778, 10.1186/s12864-015-2008-0 Roy, 1999, In vivo processing and antibiotic activity of microcin B17 analogs with varying ring content and altered bisheterocyclic sites, Chem. Biol., 6, 305, 10.1016/S1074-5521(99)80076-3 Thompson, 2014, Synthesis of full length and truncated microcin B17 analogues as DNA gyrase poisons, Org. Biomol. Chem., 12, 1570, 10.1039/C3OB42516A F. Collin, R.E. Thompson, K.A. Jolliffe, R.J. Payne, A. Maxwell, Fragments of the bacterial toxin microcin B17 as gyrase poisons., PLoS One. 8 (2013) e61459. https://doi.org/10.1371/journal.pone.0061459. I. Shkundina, M. Serebryakova, K. Severinov, The C-terminal part of microcin B is crucial for DNA gyrase inhibition and antibiotic uptake by sensitive cells., J. Bacteriol. 196 (2014) 1759–67. https://doi.org/10.1128/JB.00015-14. Lavina, 1986, Identification, mapping, cloning and characterization of a gene (sbmA) required for microcin B17 action on Escherichia coli K12, Microbiology., 132, 1685, 10.1099/00221287-132-6-1685 J. Glazebrook, A. Ichige, G.C. Walker, A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development., Genes Dev. 7 (1993) 1485–97. http://www.ncbi.nlm.nih.gov/pubmed/8393417. Pränting, 2008, Mechanism and fitness costs of PR-39 resistance in Salmonella enterica serovar Typhimurium LT2, Antimicrob. Agents Chemother., 52, 2734, 10.1128/AAC.00205-08 LeVier, 2001, Genetic analysis of the Sinorhizobium meliloti BacA protein: differential effects of mutations on phenotypes, J. Bacteriol., 183, 6444, 10.1128/JB.183.21.6444-6453.2001 G. Runti, M.d.C. Lopez Ruiz, T. Stoilova, R. Hussain, M. Jennions, H.G. Choudhury, M. Benincasa, R. Gennaro, K. Beis, M. Scocchi, Functional characterization of SbmA, a bacterial inner membrane transporter required for importing the antimicrobial peptide Bac7(1–35), J. Bacteriol. 195 (2013) 5343–5351. https://doi.org/10.1128/JB.00818-13. Corbalan, 2013, Functional and structural study of the dimeric inner membrane protein SbmA, J. Bacteriol., 195, 5352, 10.1128/JB.00824-13 Salomon, 1995, The peptide antibiotic microcin 25 is imported through the tonB pathway and the sbmA protein, J. Bacteriol., 177, 3323, 10.1128/JB.177.11.3323-3325.1995 Mattiuzzo, 2007, Role of the Escherichia coli SbmA in the antimicrobial activity of proline-rich peptides, Mol. Microbiol., 66, 151, 10.1111/j.1365-2958.2007.05903.x A. Ghosal, A. Vitali, J.E.M. Stach, P.E. Nielsen, Role of SbmA in the uptake of peptide nucleic acid (PNA)–peptide conjugates in E. coli, ACS Chem. Biol. 8 (2013) 360–367. doi:https://doi.org/10.1021/cb300434e. Puckett, 2012, Bacterial resistance to antisense peptide phosphorodiamidate morpholino oligomers, Antimicrob. Agents Chemother., 56, 6147, 10.1128/AAC.00850-12 Sato, 2000, Expression of outer membrane proteins in Escherichia coli growing at acid pH, Appl. Environ. Microbiol., 66, 943, 10.1128/AEM.66.3.943-947.2000 Benz, 1988, Structure and function of porins from gram-negative bacteria, Annu. Rev. Microbiol., 42, 359, 10.1146/annurev.mi.42.100188.002043 M.D.C. Garrido, M. Herrero, R. Kolter, F. Moreno, The export of the DNA replication inhibitor microcin B17 provides immunity for the host cell; the export of the DNA replication inhibitor Microcin B17 provides immunity for the host cell., EMBO J. 7 (1988) 853–1862. https://doi.org/10.1002/j.1460-2075.1988.tb03018.x. Vetting, 2006, Pentapeptide repeat proteins, Biochemistry., 45, 1, 10.1021/bi052130w Hashimi, 2007, The phytotoxin albicidin is a novel inhibitor of DNA gyrase, Antimicrob. Agents Chemother., 51, 181, 10.1128/AAC.00918-06 Baumann, 2014, Cystobactamids: myxobacterial topoisomerase inhibitors exhibiting potent antibacterial activity, Angew. Chemie Int. Ed., 53, 14605, 10.1002/anie.201409964 Tran, 2002, Mechanism of plasmid-mediated quinolone resistance, Proc. Natl. Acad. Sci. U. S. A., 99, 5638, 10.1073/pnas.082092899 Montero, 2001, Intrinsic resistance of Mycobacterium smegmatis to fluoroquinolones may be influenced by new pentapeptide protein MfpA, Antimicrob. Agents Chemother., 45, 3387, 10.1128/AAC.45.12.3387-3392.2001 Hegde, 2005, A fluoroquinolone resistance protein from Mycobacterium tuberculosis that mimics DNA, Science, 308, 1480, 10.1126/science.1110699 Mérens, 2009, The pentapeptide repeat proteins MfpAMt and QnrB4 exhibit opposite effects on DNA gyrase catalytic reactions and on the ternary gyrase–DNA–quinolone complex, J. Bacteriol., 191, 1587, 10.1128/JB.01205-08 Hegde, 2011, Structural and biochemical analysis of the pentapeptide repeat protein EfsQnr, a potent DNA gyrase inhibitor, Antimicrob. Agents Chemother., 55, 110, 10.1128/AAC.01158-10 Cociancich, 2015, The gyrase inhibitor albicidin consists of p-aminobenzoic acids and cyanoalanine, Nat. Chem. Biol., 11, 195, 10.1038/nchembio.1734 Vetting, 2011, Pentapeptide-repeat proteins that act as topoisomerase poison resistance factors have a common dimer interface, Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun., 67, 296, 10.1107/S1744309110053315 Tran, 2005, Interaction of the plasmid-encoded quinolone resistance protein Qnr with Escherichia coli DNA gyrase, Antimicrob. Agents Chemother., 49, 118, 10.1128/AAC.49.1.118-125.2005 Jacoby, 2015, Protective effect of qnr on agents other than quinolones that target DNA gyrase, Antimicrob. Agents Chemother., 59, 6689, 10.1128/AAC.01292-15 Hooper, 2016, Topoisomerase inhibitors: fluoroquinolone mechanisms of action and resistance, Cold Spring Harb. Perspect. Med., 6, a025320, 10.1101/cshperspect.a025320 Lomovskaya, 1996, Differential regulation of the mcb and emr operons of Escherichia coli: role of mcb in multidrug resistance, Antimicrob. Agents Chemother., 40, 1050, 10.1128/AAC.40.4.1050 Tao, 2013, Mycobacterium fluoroquinolone resistance protein B, a novel small GTPase, is involved in the regulation of DNA gyrase and drug resistance, Nucleic Acids Res., 41, 2370, 10.1093/nar/gks1351 M.R. Baquero, M. Bouzon, J. Varea, F. Moreno, sbmC, a stationary-phase induced SOS Escherichia coli gene, whose product protects cells from the DNA replication inhibitor microcin B17, Mol. Microbiol. 18 (1995) 301–311. https://doi.org/10.1111/j.1365-2958.1995.mmi_18020301.x. Nakanishi, 1998, Identification of DNA gyrase inhibitor (GyrI) in Escherichia coli, J. Biol. Chem., 273, 1933, 10.1074/jbc.273.4.1933 Nakanishi, 2002, Characterization of the interaction between DNA gyrase inhibitor and DNA gyrase of Escherichia coli, J. Biol. Chem., 277, 8949, 10.1074/jbc.M111278200 Romanowski, 2002, Crystal structure of the Escherichia coli SbmC protein that protects cells from the DNA replication inhibitor microcin B17, Proteins., 47, 403, 10.1002/prot.10102 Chatterji, 2003, Chromosomally encoded gyrase inhibitor GyrI protects Escherichia coli against DNA-damaging agents, Arch. Microbiol., 180, 339, 10.1007/s00203-003-0598-4 Shah, 2014, Squaring up to DNA: pentapeptide repeat proteins and DNA mimicry, Appl. Microbiol. Biotechnol., 98, 9545, 10.1007/s00253-014-6151-3 Del Castillo, 2001, Construction and characterization of mutations at codon 751 of the Escherichia coli gyrB gene that confer resistance to the antimicrobial peptide microcin B17 and alter the activity of DNA gyrase, J. Bacteriol., 183, 2137, 10.1128/JB.183.6.2137-2140.2001 Baquero, 1978, Microcin plasmids: a group of extrachromosomal elements coding for low-molecular-weight antibiotics in Escherichia coli, J. Bacteriol., 135, 342, 10.1128/JB.135.2.342-347.1978 San Millan, 1985, Plasmid genes required for microcin B17 production, J. Bacteriol., 163, 1016, 10.1128/JB.163.3.1016-1020.1985 Genilloud, 1989, DNA sequence, products, and transcriptional pattern of the genes involved in production of the DNA replication inhibitor microcin B17, J. Bacteriol., 171, 1126, 10.1128/JB.171.2.1126-1135.1989 Rodríguez-Sáinz, 1990, Molecular characterization of pmbA, an Escherichia coli chromosomal gene required for the production of the antibiotic peptide MccB17, Mol. Microbiol., 4, 1921, 10.1111/j.1365-2958.1990.tb02041.x A. Bayer, S. Freund, G. Jung, Post-translational heterocyclic backbone modifications in the 43-peptide antibiotic microcin B17. Structure elucidation and NMR study of a 13c,18N-labelled gyrase inhibitor, Eur. J. Biochem. 234 (1995) 414–426. https://doi.org/10.1111/j.1432-1033.1995.414_b.x. Ghilarov, 2019, Architecture of Microcin B17 Synthetase: An Octameric Protein Complex Converting a Ribosomally Synthesized Peptide into a DNA Gyrase Poison, Mol Cell, 73, 749, 10.1016/j.molcel.2018.11.032 Milne, 1999, Cofactor requirements and reconstitution of Microcin B17 synthetase: a multienzyme complex that catalyzes the formation of oxazoles and thiazoles in the antibiotic microcin B17, Biochemistry., 38, 4768, 10.1021/bi982975q Y.M. Li, J.C. Milne, L.L. Madison, R. Kolter, C.T. Walsh, From peptide precursors to oxazole and thiazole-containing peptide antibiotics: microcin B17 synthase, Science (80-. ). 274 (1996) 1188–1193. https://doi.org/10.1126/science.274.5290.1188. Zamble, 2000, The McbB component of microcin B17 synthetase is a zinc metalloprotein, Biochemistry., 39, 16190, 10.1021/bi001398e Madison, 1997, The leader peptide is essential for the post-translational modification of the DNA–gyrase inhibitor microcin B17, Mol. Microbiol., 23, 161, 10.1046/j.1365-2958.1997.2041565.x Houssen, 2010, Solution structure of the leader sequence of the patellamide precursor peptide, PatE1–34, ChemBioChem., 11, 1867, 10.1002/cbic.201000305 Koehnke, 2015, Structural analysis of leader peptide binding enables leader-free cyanobactin processing, Nat. Chem. Biol., 11, 558, 10.1038/nchembio.1841 Sinha Roy, 1998, Role of the microcin B17 propeptide in substrate recognition: solution structure and mutational analysis of McbA1–26, Chem. Biol., 5, 217, 10.1016/S1074-5521(98)90635-4 B.J. Burkhart, C.J. Schwalen, G. Mann, J.H. Naismith, D.A. Mitchell, YcaO-dependent posttranslational amide activation: biosynthesis, structure, and function., Chem. Rev. 117 (2017) 5389–5456. https://doi.org/10.1021/acs.chemrev.6b00623. Milne, 1998, ATP/GTP hydrolysis is required for oxazole and thiazole biosynthesis in the peptide antibiotic microcin B17, Biochemistry., 37, 13250, 10.1021/bi980996e Dunbar, 2013, Insights into the mechanism of peptide cyclodehydrations achieved through the chemoenzymatic generation of amide derivatives, J. Am. Chem. Soc., 135, 8692, 10.1021/ja4029507 S.-H. Dong, A. Liu, N. Mahanta, D.A. Mitchell, S.K. Nair, Mechanistic basis for ribosomal peptide backbone modifications, ACS Cent. Sci. (2019) acscentsci.9b00124. https://doi.org/10.1021/acscentsci.9b00124. Melby, 2014, Orchestration of enzymatic processing by thiazole/oxazole-modified microcin dehydrogenases, Biochemistry., 53, 413, 10.1021/bi401529y Sinha Roy, 1998, Mutational analysis of posttranslational heterocycle biosynthesis in the gyrase inhibitor microcin B17: distance dependence from propeptide and tolerance for substitution in a GSCG cyclizable sequence, Biochemistry., 37, 4125, 10.1021/bi9728250 Kelleher, 1998, Regioselectivity and chemoselectivity analysis of oxazole and thiazole ring formation by the peptide-heterocyclizing microcin B17 synthetase using high-resolution MS/MS [19], J. Am. Chem. Soc., 120, 9716, 10.1021/ja9822097 Sinha Roy, 1999, Thiazole and oxazole peptides: biosynthesis and molecular machinery, Nat. Prod. Rep., 16, 249, 10.1039/a806930a Allali, 2002, The highly conserved TldD and TldE proteins of Escherichia coli are involved in microcin B17 processing and in CcdA degradation, J. Bacteriol., 184, 3224, 10.1128/JB.184.12.3224-3231.2002 Murayama, 1996, Evidence for involvement of Escherichia coli genes pmbA, csrA and a previously unrecognized gene tldD, in the control of DNA gyrase by letD (ccdB) of sex factor F, J. Mol. Biol., 256, 483, 10.1006/jmbi.1996.0103 D. Ghilarov, M. Serebryakova, C.E.M. Stevenson, S.J. Hearnshaw, D.S. Volkov, A. Maxwell, D.M. Lawson, K. Severinov, The origins of specificity in the microcin-processing protease TldD/E., Structure. 25 (2017) 1549–1561.e5. https://doi.org/10.1016/j.str.2017.08.006. S.S. Iyer, T. Gensollen, A. Gandhi, S.F. Oh, J.F. Neves, F. Collin, R. Lavin, C. Serra, J. Glickman, P.S.A. de Silva, R.B. Sartor, G. Besra, R. Hauser, A. Maxwell, A. Llebaria, R.S. Blumberg, Dietary and microbial oxazoles induce intestinal inflammation by modulating aryl hydrocarbon receptor responses., Cell. 173 (2018) 1123–1134.e11. https://doi.org/10.1016/j.cell.2018.04.037. Arrieta, 2014, The intestinal microbiome in early life: health and disease, Front. Immunol., 5, 427, 10.3389/fimmu.2014.00427 Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome., Nature. 486 (2012) 207–14. https://doi.org/10.1038/nature11234. Human Microbiome Project Consortium. A framework for human microbiome research., Nature. 486 (2012) 215–21. https://doi.org/10.1038/nature11209. van Hemert, 2010, Identification of Lactobacillus plantarum genes modulating the cytokine response of human peripheral blood mononuclear cells, BMC Microbiol., 10, 293, 10.1186/1471-2180-10-293 Flaherty, 2014, The wide world of ribosomally encoded bacterial peptides, PLoS Pathog., 10, 10.1371/journal.ppat.1004221 Wirtz, 2007, Mouse models of inflammatory bowel disease, Adv. Drug Deliv. Rev., 59, 1073, 10.1016/j.addr.2007.07.003 Wirtz, 2007, Chemically induced mouse models of intestinal inflammation, Nat. Protoc., 2, 541, 10.1038/nprot.2007.41 Van Melderen, 2001, Molecular interactions of the CcdB poison with its bacterial target, the DNA gyrase, Int. J. Med. Microbiol., 291, 537, 10.1078/1438-4221-00164 M. Metelev, I.A. Osterman, D. Ghilarov, N.F. Khabibullina, A. Yakimov, K. Shabalin, I. Utkina, D.Y. Travin, E.S. Komarova, M. Serebryakova, T. Artamonova, M. Khodorkovskii, A.L. Konevega, P.V. Sergiev, K. Severinov, Y.S. Polikanov, Klebsazolicin inhibits 70S ribosome by obstructing the peptide exit tunnel., Nat. Chem. Biol. 13 (2017) 1129–1136. https://doi.org/10.1038/nchembio.2462. Baindara, 2018, Bacteriocins: perspective for the development of novel anticancer drugs, Appl. Microbiol. Biotechnol., 102, 10393, 10.1007/s00253-018-9420-8 Travin, 2018, Biosynthesis of translation inhibitor klebsazolicin proceeds through heterocyclization and N-terminal amidine formation catalyzed by a single YcaO enzyme, J. Am. Chem. Soc., 140, 5625, 10.1021/jacs.8b02277 McIntosh, 2010, Circular logic: nonribosomal peptide-like macrocyclization with a ribosomal peptide catalyst, J. Am. Chem. Soc., 132, 15499, 10.1021/ja1067806 Chan, 2015, Structural basis of DNA gyrase inhibition by antibacterial QPT-1, anticancer drug etoposide and moxifloxacin, Nat. Commun., 6, 10048, 10.1038/ncomms10048 Rudolph, 2013, Mapping the spectrum of conformational states of the DNA- and C-gates in Bacillus subtilis gyrase, J. Mol. Biol., 425, 2632, 10.1016/j.jmb.2013.04.010