High-resolution landscape of an antibiotic binding site.
Anti-Bacterial Agents
/ chemistry
Binding Sites
/ drug effects
DNA Breaks
/ drug effects
DNA Replication
/ drug effects
DNA-Directed RNA Polymerases
/ antagonists & inhibitors
Drug Resistance, Bacterial
/ genetics
Escherichia coli
/ drug effects
Mutation
Nucleotides
/ deficiency
Promoter Regions, Genetic
Rifampin
/ chemistry
Time Factors
Transcription, Genetic
/ drug effects
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
Oct 2023
Oct 2023
Historique:
received:
03
08
2022
accepted:
28
07
2023
medline:
23
10
2023
pubmed:
31
8
2023
entrez:
30
8
2023
Statut:
ppublish
Résumé
Antibiotic binding sites are located in important domains of essential enzymes and have been extensively studied in the context of resistance mutations; however, their study is limited by positive selection. Using multiplex genome engineering
Identifiants
pubmed: 37648864
doi: 10.1038/s41586-023-06495-6
pii: 10.1038/s41586-023-06495-6
pmc: PMC10550828
mid: NIHMS1934864
doi:
Substances chimiques
Anti-Bacterial Agents
0
DNA-Directed RNA Polymerases
EC 2.7.7.6
Nucleotides
0
Rifampin
VJT6J7R4TR
sporulation-specific sigma factors
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
180-187Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM126891
Pays : United States
Organisme : NIAID NIH HHS
ID : T32 AI007180
Pays : United States
Informations de copyright
© 2023. The Author(s).
Références
Wang, H. H. et al. Programming cells by multiplex genome engineering and accelerated evolution. Nature 460, 894–898 (2009).
pubmed: 19633652
pmcid: 4590770
doi: 10.1038/nature08187
Imamovic, L. & Sommer, M. O. A. Use of collateral sensitivity networks to design drug cycling protocols that avoid resistance development. Sci. Transl. Med. 5, 204ra132 (2013).
pubmed: 24068739
doi: 10.1126/scitranslmed.3006609
Baym, M., Stone, L. K. & Kishony, R. Multidrug evolutionary strategies to reverse antibiotic resistance. Science 351, aad3292 (2016).
pubmed: 26722002
pmcid: 5496981
doi: 10.1126/science.aad3292
Rasouly, A. et al. Analysing the fitness cost of antibiotic resistance to identify targets for combination antimicrobials. Nat Microbiol 6, 1410–1423 (2021).
pubmed: 34697460
pmcid: 9389595
doi: 10.1038/s41564-021-00973-1
Freedy, A. M. & Liau, B. B. Discovering new biology with drug-resistance alleles. Nat. Chem. Biol. 17, 1219–1229 (2021).
pubmed: 34799733
pmcid: 9530778
doi: 10.1038/s41589-021-00865-9
Ezekiel, D. H. & Hutchins, J. E. Mutations affecting RNA polymerase associated with rifampicin resistance in Escherichia coli. Nature 220, 276–277 (1968).
pubmed: 4879326
doi: 10.1038/220276a0
Jin, D. J. & Gross, C. A. Characterization of the pleiotropic phenotypes of rifampin-resistant rpoB mutants of Escherichia coli. J. Bacteriol. 171, 5229–5231 (1989).
pubmed: 2670912
pmcid: 210350
doi: 10.1128/jb.171.9.5229-5231.1989
Campbell, E. A. et al. Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 104, 901–912 (2001).
pubmed: 11290327
doi: 10.1016/S0092-8674(01)00286-0
Goldstein, B. P. Resistance to rifampicin: a review. J. Antibiot. 67, 625–630 (2014).
doi: 10.1038/ja.2014.107
Molodtsov, V., Scharf, N. T., Stefan, M. A., Garcia, G. A. & Murakami, K. S. Structural basis for rifamycin resistance of bacterial RNA polymerase by the three most clinically important RpoB mutations found in Mycobacterium tuberculosis. Mol. Microbiol. 103, 1034–1045 (2017).
pubmed: 28009073
pmcid: 5344776
doi: 10.1111/mmi.13606
Ozaki, M., Mizushima, S. & Nomura, M. Identification and functional characterization of the protein controlled by the streptomycin-resistant locus in E. coli. Nature 222, 333–339 (1969).
pubmed: 4181187
doi: 10.1038/222333a0
Galas, D. J. & Branscomb, E. W. Ribosome slowed by mutation to streptomycin resistance. Nature 262, 617–619 (1976).
pubmed: 785282
doi: 10.1038/262617b0
Zhang, Y. et al. The context of the ribosome binding site in mRNAs defines specificity of action of kasugamycin, an inhibitor of translation initiation. Proc. Natl Acad. Sci. USA 119, e2118553119 (2022).
pubmed: 35064089
pmcid: 8794815
doi: 10.1073/pnas.2118553119
Svetlov, M. S., Vázquez-Laslop, N. & Mankin, A. S. Kinetics of drug-ribosome interactions defines the cidality of macrolide antibiotics. Proc. Natl Acad. Sci. USA 114, 13673–13678 (2017).
pubmed: 29229833
pmcid: 5748224
doi: 10.1073/pnas.1717168115
McDowell, J. C., Roberts, J. W., Jin, D. J. & Gross, C. Determination of intrinsic transcription termination efficiency by RNA polymerase elongation rate. Science 266, 822–825 (1994).
pubmed: 7526463
doi: 10.1126/science.7526463
Zhou, Y. N. & Jin, D. J. The rpoB mutants destabilizing initiation complexes at stringently controlled promoters behave like ‘stringent’ RNA polymerases in Escherichia coli. Proc. Natl Acad. Sci. USA 95, 2908–2913 (1998).
pubmed: 9501189
pmcid: 19668
doi: 10.1073/pnas.95.6.2908
Fredriksson, A., Ballesteros, M., Dukan, S. & Nyström, T. Induction of the heat shock regulon in response to increased mistranslation requires oxidative modification of the malformed proteins. Mol. Microbiol. 59, 350–359 (2006).
pubmed: 16359340
doi: 10.1111/j.1365-2958.2005.04947.x
Saito, K. et al. Rifamycin action on RNA polymerase in antibiotic-tolerant Mycobacterium tuberculosis results in differentially detectable populations. Proc. Natl Acad. Sci. USA 114, E4832–E4840 (2017).
pubmed: 28559332
pmcid: 5474769
doi: 10.1073/pnas.1705385114
Lin, W. et al. Structural basis of Mycobacterium tuberculosis transcription and transcription inhibition. Mol. Cell 66, 169–179.e8 (2017).
pubmed: 28392175
pmcid: 5438085
doi: 10.1016/j.molcel.2017.03.001
Jin, D. J. & Gross, C. A. Mapping and sequencing of mutations in the Escherichia coli rpoB gene that lead to rifampicin resistance. J. Mol. Biol. 202, 45–58 (1988).
pubmed: 3050121
doi: 10.1016/0022-2836(88)90517-7
Svetlov, V., Belogurov, G. A., Shabrova, E., Vassylyev, D. G. & Artsimovitch, I. Allosteric control of the RNA polymerase by the elongation factor RfaH. Nucleic Acids Res. 35, 5694–5705 (2007).
pubmed: 17711918
pmcid: 2034486
doi: 10.1093/nar/gkm600
Jin, D. J. et al. Effects of rifampicin resistant rpoB mutations on antitermination and interaction with nusA in Escherichia coli. J. Mol. Biol. 204, 247–261 (1988).
pubmed: 2464690
doi: 10.1016/0022-2836(88)90573-6
Yanofsky, C. & Horn, V. Rifampin resistance mutations that alter the efficiency of transcription termination at the tryptophan operon attenuator. J. Bacteriol. 145, 1334–1341 (1981).
pubmed: 7009579
pmcid: 217137
doi: 10.1128/jb.145.3.1334-1341.1981
Shiver, A. L. et al. Chemical-genetic interrogation of RNA polymerase mutants reveals structure-function relationships and physiological tradeoffs. Mol Cell 81, 2201–2215.e9 (2021).
pubmed: 34019789
pmcid: 8484514
doi: 10.1016/j.molcel.2021.04.027
Jee, J. et al. Rates and mechanisms of bacterial mutagenesis from maximum-depth sequencing. Nature 534, 693–696 (2016).
pubmed: 27338792
pmcid: 4940094
doi: 10.1038/nature18313
Adams, R. A. et al. Rifamycin antibiotics and the mechanisms of their failure. J. Antibiot. 74, 786–798 (2021).
doi: 10.1038/s41429-021-00462-x
Kelsic, E. D. et al. RNA structural determinants of optimal codons revealed by MAGE-Seq. Cell Systems 3, 563–571.e6 (2016).
pubmed: 28009265
pmcid: 5234859
doi: 10.1016/j.cels.2016.11.004
Park, J. & Wang, H. H. Systematic dissection of σ70 sequence diversity and function in bacteria. Cell Rep 36, 109590 (2021).
pubmed: 34433066
pmcid: 8716302
doi: 10.1016/j.celrep.2021.109590
Russ, D. et al. Escape mutations circumvent a tradeoff between resistance to a beta-lactam and resistance to a beta-lactamase inhibitor. Nat. Commun. 11, 2029 (2020).
pubmed: 32332717
pmcid: 7181632
doi: 10.1038/s41467-020-15666-2
Ellis, H. M., Yu, D., DiTizio, T. & Court, D. L. High efficiency mutagenesis, repair, and engineering of chromosomal DNA using single-stranded oligonucleotides. Proc. Natl Acad. Sci. USA 98, 6742–6746 (2001).
pubmed: 11381128
pmcid: 34423
doi: 10.1073/pnas.121164898
Nyerges, Á. et al. Directed evolution of multiple genomic loci allows the prediction of antibiotic resistance. Proc. Natl Acad. Sci. USA 115, E5726–E5735 (2018).
pubmed: 29871954
pmcid: 6016788
doi: 10.1073/pnas.1801646115
Jin, D. J., Burgess, R. R., Richardson, J. P. & Gross, C. A. Termination efficiency at rho-dependent terminators depends on kinetic coupling between RNA polymerase and rho. Proc. Natl Acad. Sci. USA 89, 1453–1457 (1992).
pubmed: 1741399
pmcid: 48469
doi: 10.1073/pnas.89.4.1453
Liu, A. et al. Antibiotic sensitivity profiles determined with an Escherichia coli gene knockout collection: generating an antibiotic bar code. Antimicrob. Agents Chemother. 54, 1393–1403 (2010).
pubmed: 20065048
pmcid: 2849384
doi: 10.1128/AAC.00906-09
Gavrieli, Y., Sherman, Y. & Ben-Sasson, S. A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493–501 (1992).
pubmed: 1400587
doi: 10.1083/jcb.119.3.493
Dwyer, D. J., Camacho, D. M., Kohanski, M. A., Callura, J. M. & Collins, J. J. Antibiotic-induced bacterial cell death exhibits physiological and biochemical hallmarks of apoptosis. Mol Cell 46, 561–572 (2012).
pubmed: 22633370
pmcid: 3710583
doi: 10.1016/j.molcel.2012.04.027
Lobritz, M. A. et al. Antibiotic efficacy is linked to bacterial cellular respiration. Proc. Natl Acad. Sci. USA 112, 8173–8180 (2015).
pubmed: 26100898
pmcid: 4500273
doi: 10.1073/pnas.1509743112
Kohanski, M. A., Dwyer, D. J., Hayete, B., Lawrence, C. A. & Collins, J. J. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130, 797–810 (2007).
pubmed: 17803904
doi: 10.1016/j.cell.2007.06.049
Rothfuss, O., Gasser, T. & Patenge, N. Analysis of differential DNA damage in the mitochondrial genome employing a semi-long run real-time PCR approach. Nucleic Acids Res. 38, e24 (2010).
pubmed: 19966269
doi: 10.1093/nar/gkp1082
Tehranchi, A. K. et al. The transcription factor DksA prevents conflicts between DNA replication and transcription machinery. Cell 141, 595–605 (2010).
pubmed: 20478253
pmcid: 2919171
doi: 10.1016/j.cell.2010.03.036
Mirkin, E. V., Castro Roa, D., Nudler, E. & Mirkin, S. M. Transcription regulatory elements are punctuation marks for DNA replication. Proc. Natl Acad. Sci. USA 103, 7276–7281 (2006).
pubmed: 16670199
pmcid: 1464333
doi: 10.1073/pnas.0601127103
Wiktor, J., Lesterlin, C., Sherratt, D. J. & Dekker, C. CRISPR-mediated control of the bacterial initiation of replication. Nucleic Acids Res. 44, 3801–3810 (2016).
pubmed: 27036863
pmcid: 4857001
doi: 10.1093/nar/gkw214
Carl, P. L. Escherichia coli mutants with temperature-sensitive synthesis of DNA. Mol Gen Genet 109, 107–122 (1970).
pubmed: 4925091
doi: 10.1007/BF00269647
Zhu, M., Mori, M., Hwa, T. & Dai, X. Disruption of transcription–translation coordination in Escherichia coli leads to premature transcriptional termination. Nat Microbiol 4, 2347–2356 (2019).
pubmed: 31451774
pmcid: 6903697
doi: 10.1038/s41564-019-0543-1
Rosener, B. et al. Evolved bacterial resistance against fluoropyrimidines can lower chemotherapy impact in the Caenorhabditis elegans host. eLife 9, e59831 (2020).
Scott, T. A. et al. Host-microbe co-metabolism dictates cancer drug efficacy in C. elegans. Cell 169, 442–456.e18 (2017).
pubmed: 28431245
pmcid: 5406385
doi: 10.1016/j.cell.2017.03.040
Rao, T. V. P. & Kuzminov, A. Exopolysaccharide defects cause hyper-thymineless death in Escherichia coli via massive loss of chromosomal DNA and cell lysis. Proc. Natl Acad. Sci. USA 117, 33549–33560 (2020).
pubmed: 33318216
pmcid: 7777189
doi: 10.1073/pnas.2012254117
Artsimovitch, I. & Landick, R. Pausing by bacterial RNA polymerase is mediated by mechanistically distinct classes of signals. Proc. Natl Acad. Sci. USA 97, 7090–7095 (2000).
pubmed: 10860976
pmcid: 16504
doi: 10.1073/pnas.97.13.7090
Giroux, X., Su, W.-L., Bredeche, M.-F. & Matic, I. Maladaptive DNA repair is the ultimate contributor to the death of trimethoprim-treated cells under aerobic and anaerobic conditions. Proc. Natl Acad. Sci. USA 114, 11512–11517 (2017).
pubmed: 29073080
pmcid: 5664507
doi: 10.1073/pnas.1706236114
Kanehisa, M., Sato, Y., Kawashima, M., Furumichi, M. & Tanabe, M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 44, D457–D462 (2016).
pubmed: 26476454
doi: 10.1093/nar/gkv1070
Capra, J. A. & Singh, M. Predicting functionally important residues from sequence conservation. Bioinformatics 23, 1875–1882 (2007).
pubmed: 17519246
doi: 10.1093/bioinformatics/btm270
Miller, W. G. et al. The complete genome sequence and analysis of the Epsilonproteobacterium Arcobacter butzleri. PLoS ONE 2, e1358 (2007).
pubmed: 18159241
pmcid: 2147049
doi: 10.1371/journal.pone.0001358
Svetlov, M. S., Cohen, S., Alsuhebany, N., Vázquez-Laslop, N. & Mankin, A. S. A long-distance rRNA base pair impacts the ability of macrolide antibiotics to kill bacteria. Proc. Natl Acad. Sci. USA 117, 1971–1975 (2020).
pubmed: 31932436
pmcid: 6995004
doi: 10.1073/pnas.1918948117
Conrad, T. M. et al. RNA polymerase mutants found through adaptive evolution reprogram Escherichia coli for optimal growth in minimal media. Proc. Natl Acad. Sci. USA 107, 20500–20505 (2010).
pubmed: 21057108
pmcid: 2996682
doi: 10.1073/pnas.0911253107
Cohen, S. S., Flaks, J. G., Barner, H. D., Loeb, M. R. & Lichtenstein, J. The mode of action of 5-fluorouracil and its derivatives. Proc. Natl Acad. Sci. USA 44, 1004–1012 (1958).
pubmed: 16590300
pmcid: 528686
doi: 10.1073/pnas.44.10.1004
Guegler, C. K. & Laub, M. T. Shutoff of host transcription triggers a toxin-antitoxin system to cleave phage RNA and abort infection. Mol Cell 81, 2361–2373.e9 (2021).
pubmed: 33838104
pmcid: 8284924
doi: 10.1016/j.molcel.2021.03.027
Chan, C. Y., Au-Yeang, C., Yew, W. W., Hui, M. & Cheng, A. F. Postantibiotic effects of antituberculosis agents alone and in combination. Antimicrob. Agents Chemother. 45, 3631–3634 (2001).
pubmed: 11709357
pmcid: 90886
doi: 10.1128/AAC.45.12.3631-3634.2001
Malik, M. et al. Lethal synergy involving bicyclomycin: an approach for reviving old antibiotics. J. Antimicrob. Chemother. 69, 3227–3235 (2014).
pubmed: 25085655
pmcid: 4228776
doi: 10.1093/jac/dku285
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 10–12 (2011).
doi: 10.14806/ej.17.1.200
Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA 97, 6640–6645 (2000).
pubmed: 10829079
pmcid: 18686
doi: 10.1073/pnas.120163297
Wiegand, I., Hilpert, K. & Hancock, R. E. W. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 3, 163–175 (2008).
pubmed: 18274517
doi: 10.1038/nprot.2007.521
Svetlov, V. & Artsimovitch, I. Purification of bacterial RNA polymerase: tools and protocols. Methods Mol. Biol. 1276, 13–29 (2015).
pubmed: 25665556
pmcid: 4324551
doi: 10.1007/978-1-4939-2392-2_2
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
pubmed: 22388286
pmcid: 3322381
doi: 10.1038/nmeth.1923
Ramírez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 44, W160–W165 (2016).
pubmed: 27079975
pmcid: 4987876
doi: 10.1093/nar/gkw257
Sikorsky, J. A., Primerano, D. A., Fenger, T. W. & Denvir, J. DNA damage reduces Taq DNA polymerase fidelity and PCR amplification efficiency. Biochem. Biophys. Res. Commun. 355, 431–437 (2007).
pubmed: 17303074
pmcid: 1945218
doi: 10.1016/j.bbrc.2007.01.169
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8
Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).
pubmed: 21988835
pmcid: 3261699
doi: 10.1038/msb.2011.75