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Research article

References

  1. Abraham EP, Chain E. 1940. An enzyme from bacteria able to destroy penicillin. Rev. Infect. Dis. 10: 677-678.
    CrossRef
  2. Bhaya D, Davison M, Barrangou R. 2011. CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet. 45: 273297.
    Pubmed CrossRef
  3. Bikard D, Euler CW, Jiang W, Nussenzweig PM, Goldberg GW, Duportet X, et al. 2014. Exploiting CRISPR-Cas nucleases to produce sequence-specific antimicrobials. Nat. Biotechnol. 32: 1146-1150.
    Pubmed PMC CrossRef
  4. Butler MS, Blaskovich MA, Cooper MA. 2013. Antibiotics in the clinical pipeline in 2013. J. Antibiot. 66: 571-591.
    Pubmed CrossRef
  5. Citorik RJ, Mimee M, Lu TK. 2014. Sequence-specific antimicrobials using efficiently delivered RNA-guided nucleases. Nat. Biotechnol. 32: 1141-1145.
    Pubmed PMC CrossRef
  6. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, et al. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819-823.
    Pubmed PMC CrossRef
  7. Fleming A. 1929. On the antibacterial action of cultures of a penicillium, with special reference to their use in the isolation of B. influenzæ. Br. J. Exp. Pathol. 10: 226-236.
    PMC
  8. Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA. 2013. RNA-guided editing of bacterial genomes using CRISPRCas systems. Nat. Biotechnol. 31: 233-239.
    Pubmed PMC CrossRef
  9. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816-821.
    Pubmed CrossRef
  10. Jones CH, Tuckman M, Keeney D, Ruzin A, Bradford PA. 2009. Characterization and sequence analysis of extendedspectrumb-lactamase-encoding genes from Escherichia coli, Klebsiella pneumoniae, and Proteus mirabilis isolates collected during tigecycline phase 3 clinical trials. Antimicrob. Agents Chemother. 53: 465-475.
    Pubmed PMC CrossRef
  11. Kaur M, Aggarwal A. 2013. Occurrence of the CTX-M, SHV and the TEM genes among the extended spectrum betalactamase producing isolates of Enterobacteriaceae in a tertiary care hospital of North India. J. Clin. Diagn. Res. 7:642-645.
    Pubmed PMC
  12. Knothe H, Shah P, Krcmery V, Antal M, Mitsuhashi S. 1983. Transferable resistance to cefotaxime, cefoxitin, cefamandole and cefuroxime in clinical isolates of Klebsiella pneumoniae and Serratia marcescens. Infection 11: 315-317.
    Pubmed CrossRef
  13. Lew W, Pai M, Oxlade O, Martin D, Menzies D. 2008. Initial drug resistance and tuberculosis treatment outcomes:systematic review and meta-analysis. Ann. Intern. Med. 149:123-134.
    Pubmed CrossRef
  14. Paterson DL. 2000. Recommendation for treatment of severe infections caused by Enterobacteriaceae producing extendedspectrum beta-lactamases (ESBLs). Clin. Microbiol. Infect. 6:460-463.
    Pubmed CrossRef
  15. Paterson DL, Bonomo RA. 2005. Extended-spectrum betalactamases:a clinical update. Clin. Microbiol. Rev. 18: 657-686.
    Pubmed PMC CrossRef
  16. Rawat D, Nair D. 2010. Extended-spectrum beta-lactamases in gram-negative bacteria. J. Global Infect. Dis. 2: 263-274.
    Pubmed PMC CrossRef
  17. Sanders CC, Sanders WE Jr. 1979. Emergence of resistance to cefamandole: possible role of cefoxitin-inducible betalactamases. Antimicrob. Agents Chemother. 15: 792-797.
    Pubmed PMC CrossRef
  18. Tissera S, Lee SM. 2013. Isolation of extended spectrum beta-lactamase (ESBL) producing bacteria from urban surface waters in Malaysia. Malays. J. Med. Sci. 20: 14-22.
    Pubmed PMC
  19. van der Oost J, Westra ER, Jackson RN, Wiedenheft B. 2014. Unravelling the structural and mechanistic basis of CRISPRCas systems. Nat. Rev. Microbiol. 12: 479-492.
    Pubmed PMC CrossRef
  20. Walsh CT, Wencewicz TA. 2014. Prospects for new antibiotics: a molecule-centered perspective. J. Antibiot. 67:7-22.
    Pubmed CrossRef
  21. Wiedenheft B, Sternberg SH, Doudna JA. 2012. RNA-guided genetic silencing systems in bacteria and archaea. Nature 482: 331-338.
    Pubmed CrossRef
  22. Wise R. 2002. Antimicrobial resistance: priorities for action. J. Antimicrob. Chemother. 49: 585-586.
    Pubmed CrossRef
  23. Woodford N, Livermore DM. 2009. Infections caused by gram-positive bacteria: a review of the global challenge. J . Infect. 59 (Suppl 1): S4-S16.
    CrossRef
  24. Yosef I, Manor M, Kiro R, Qimron U. 2015. Temperate and lytic bacteriophages programmed to sensitize and kill antibiotic-resistant bacteria. Proc. Natl. Acad. Sci. USA 112:7267-7272.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(2): 394-401

Published online February 28, 2016 https://doi.org/10.4014/jmb.1508.08080

Copyright © The Korean Society for Microbiology and Biotechnology.

CRISPR/Cas9-Mediated Re-Sensitization of Antibiotic-Resistant Escherichia coli Harboring Extended-Spectrum β-Lactamases

Jun-Seob Kim 1, 2, Da-Hyeong Cho 1, Myeongseo Park 1, Woo-Jae Chung 1, Dongwoo Shin 3, Kwan Soo Ko 3 and Dae-Hyuk Kweon 1*

1Department of Genetic Engineering and Center for Human Interface Nano Technology, Sungkyunkwan University, Suwon 16419, Republic of Korea, 2Department of Food Science and Human Nutrition, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA, 3Department of Molecular Cell Biology, Sungkyunkwan University School of Medicine, Suwon 16419, Republic of Korea

Received: August 28, 2015; Accepted: October 23, 2015

Abstract

Recently, the clustered regularly interspaced short palindromic repeats (CRISPR)-associated
protein 9 (CRISPR/Cas9) system, a genome editing technology, was shown to be versatile in
treating several antibiotic-resistant bacteria. In the present study, we applied the CRISPR/
Cas9 technology to kill extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli.
ESBL bacteria are mostly multidrug resistant (MDR), and have plasmid-mediated antibiotic
resistance genes that can be easily transferred to other members of the bacterial community by
horizontal gene transfer. To restore sensitivity to antibiotics in these bacteria, we searched for
a CRISPR/Cas9 target sequence that was conserved among >1,000 ESBL mutants. There was
only one target sequence for each TEM- and SHV-type ESBL, with each of these sequences
found in ~200 ESBL strains of each type. Furthermore, we showed that these target sequences
can be exploited to re-sensitize MDR cells in which resistance is mediated by genes that are not
the target of the CRISPR/Cas9 system, but by genes that are present on the same plasmid as
target genes. We believe our Re-Sensitization to Antibiotics from Resistance (ReSAFR)
technology, which enhances the practical value of the CRISPR/Cas9 system, will be an
effective method of treatment against plasmid-carrying MDR bacteria.

Keywords: Extended spectrum beta-lactamases (ESBLs), Multi-drug resistance (MDR), Re-sensitization, CRISPR/Cas9, Antibiotic resistance

References

  1. Abraham EP, Chain E. 1940. An enzyme from bacteria able to destroy penicillin. Rev. Infect. Dis. 10: 677-678.
    CrossRef
  2. Bhaya D, Davison M, Barrangou R. 2011. CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet. 45: 273297.
    Pubmed CrossRef
  3. Bikard D, Euler CW, Jiang W, Nussenzweig PM, Goldberg GW, Duportet X, et al. 2014. Exploiting CRISPR-Cas nucleases to produce sequence-specific antimicrobials. Nat. Biotechnol. 32: 1146-1150.
    Pubmed KoreaMed CrossRef
  4. Butler MS, Blaskovich MA, Cooper MA. 2013. Antibiotics in the clinical pipeline in 2013. J. Antibiot. 66: 571-591.
    Pubmed CrossRef
  5. Citorik RJ, Mimee M, Lu TK. 2014. Sequence-specific antimicrobials using efficiently delivered RNA-guided nucleases. Nat. Biotechnol. 32: 1141-1145.
    Pubmed KoreaMed CrossRef
  6. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, et al. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819-823.
    Pubmed KoreaMed CrossRef
  7. Fleming A. 1929. On the antibacterial action of cultures of a penicillium, with special reference to their use in the isolation of B. influenzæ. Br. J. Exp. Pathol. 10: 226-236.
    KoreaMed
  8. Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA. 2013. RNA-guided editing of bacterial genomes using CRISPRCas systems. Nat. Biotechnol. 31: 233-239.
    Pubmed KoreaMed CrossRef
  9. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816-821.
    Pubmed CrossRef
  10. Jones CH, Tuckman M, Keeney D, Ruzin A, Bradford PA. 2009. Characterization and sequence analysis of extendedspectrumb-lactamase-encoding genes from Escherichia coli, Klebsiella pneumoniae, and Proteus mirabilis isolates collected during tigecycline phase 3 clinical trials. Antimicrob. Agents Chemother. 53: 465-475.
    Pubmed KoreaMed CrossRef
  11. Kaur M, Aggarwal A. 2013. Occurrence of the CTX-M, SHV and the TEM genes among the extended spectrum betalactamase producing isolates of Enterobacteriaceae in a tertiary care hospital of North India. J. Clin. Diagn. Res. 7:642-645.
    Pubmed KoreaMed
  12. Knothe H, Shah P, Krcmery V, Antal M, Mitsuhashi S. 1983. Transferable resistance to cefotaxime, cefoxitin, cefamandole and cefuroxime in clinical isolates of Klebsiella pneumoniae and Serratia marcescens. Infection 11: 315-317.
    Pubmed CrossRef
  13. Lew W, Pai M, Oxlade O, Martin D, Menzies D. 2008. Initial drug resistance and tuberculosis treatment outcomes:systematic review and meta-analysis. Ann. Intern. Med. 149:123-134.
    Pubmed CrossRef
  14. Paterson DL. 2000. Recommendation for treatment of severe infections caused by Enterobacteriaceae producing extendedspectrum beta-lactamases (ESBLs). Clin. Microbiol. Infect. 6:460-463.
    Pubmed CrossRef
  15. Paterson DL, Bonomo RA. 2005. Extended-spectrum betalactamases:a clinical update. Clin. Microbiol. Rev. 18: 657-686.
    Pubmed KoreaMed CrossRef
  16. Rawat D, Nair D. 2010. Extended-spectrum beta-lactamases in gram-negative bacteria. J. Global Infect. Dis. 2: 263-274.
    Pubmed KoreaMed CrossRef
  17. Sanders CC, Sanders WE Jr. 1979. Emergence of resistance to cefamandole: possible role of cefoxitin-inducible betalactamases. Antimicrob. Agents Chemother. 15: 792-797.
    Pubmed KoreaMed CrossRef
  18. Tissera S, Lee SM. 2013. Isolation of extended spectrum beta-lactamase (ESBL) producing bacteria from urban surface waters in Malaysia. Malays. J. Med. Sci. 20: 14-22.
    Pubmed KoreaMed
  19. van der Oost J, Westra ER, Jackson RN, Wiedenheft B. 2014. Unravelling the structural and mechanistic basis of CRISPRCas systems. Nat. Rev. Microbiol. 12: 479-492.
    Pubmed KoreaMed CrossRef
  20. Walsh CT, Wencewicz TA. 2014. Prospects for new antibiotics: a molecule-centered perspective. J. Antibiot. 67:7-22.
    Pubmed CrossRef
  21. Wiedenheft B, Sternberg SH, Doudna JA. 2012. RNA-guided genetic silencing systems in bacteria and archaea. Nature 482: 331-338.
    Pubmed CrossRef
  22. Wise R. 2002. Antimicrobial resistance: priorities for action. J. Antimicrob. Chemother. 49: 585-586.
    Pubmed CrossRef
  23. Woodford N, Livermore DM. 2009. Infections caused by gram-positive bacteria: a review of the global challenge. J . Infect. 59 (Suppl 1): S4-S16.
    CrossRef
  24. Yosef I, Manor M, Kiro R, Qimron U. 2015. Temperate and lytic bacteriophages programmed to sensitize and kill antibiotic-resistant bacteria. Proc. Natl. Acad. Sci. USA 112:7267-7272.
    Pubmed KoreaMed CrossRef