CRISPR/Cas9-mediated phage resistance is not impeded by the DNA modifications of phage T4

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Yaung, Stephanie J ^a,b   Esvelt, Kevin M ^a   Church, George M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLCYTOSINE; 6 N METHYLADENINE; CAS9 NUCLEASE; CYTOSINE; NUCLEASE; UNCLASSIFIED DRUG; 5-HYDROXYMETHYLCYTOSINE; BACTERIAL DNA; CRISPR ASSOCIATED PROTEIN; ENDONUCLEASE;

ARTICLE; BACTERIOPHAGE T4; BIOINFORMATICS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; DNA METHYLATION; DNA MODIFICATION; ESCHERICHIA COLI; GENE TARGETING; GENETIC TRANSFORMATION; GLYCOSYLATION; MACROPHAGE FUNCTION; MACROPHAGE RESISTANCE; NONHUMAN; STREPTOCOCCUS PYOGENES; ANALOGS AND DERIVATIVES; CHEMISTRY; CRISPR CAS SYSTEM; ENTEROBACTERIA PHAGE T4; GENETICS; METABOLISM; VIROLOGY;

5-METHYLCYTOSINE; BACTERIOPHAGE T4; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; CYTOSINE; DNA, BACTERIAL; ENDONUCLEASES; ESCHERICHIA COLI; STREPTOCOCCUS PYOGENES;

EID: 84902338476     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098811     Document Type: Article

References (33)

1. Lehman IR, Pratt EA (1960) On the structure of the glucosylated hydroxymethylcytosine nucleotides of coliphages T2, T4, and T6. J Biol Chem 235: 3254-3259.
2. Kelleher J, Raleigh E (1991) A novel activity in Escherichia coli K-12 that directs restriction of DNA modified at CG dinucleotides. J Bacteriol 173: 5220-5223.
3. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, et al. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816-821. doi:10.1126/science.1225829.
4. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, et al. (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science (80-) 315: 1709-1712. doi:10.1126/science.1138140.
5. Marraffini LA, Sontheimer EJ (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322: 1843-1845. doi:10.1126/science.1165771.
6. Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, et al. (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471: 602-607. doi:10.1038/nature09886.
7. Mojica FJM, Díez-Villaseñor C, García-Martínez J, Almendros C (2009) Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 155: 733-740. doi:10.1099/mic.0.023960-0.
8. Grissa I, Vergnaud G, Pourcel C (2007) The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics 8: 172. doi:10.1186/1471-2105-8-172.
9. Díez-Villaseñor C, Almendros C, García- Martínez J, Mojica FJM (2010) Diversity of CRISPR loci in Escherichia coli. Microbiology 156: 1351-1361. doi:10.1099/mic.0.036046-0.
10. Touchon M, Charpentier S, Clermont O, Rocha EPC, Denamur E, et al. (2011) CRISPR distribution within the Escherichia coli species is not suggestive of immunity-associated diversifying selection. J Bacteriol 193: 2460-2467. doi:10.1128/JB.01307-10.
11. Toro M, Cao G, Ju W, Allard M, Barrangou R, et al. (2014) Association of Clustered Regularly Interspaced Short Palindromic Repeat (CRISPR) Elements with Specific Serotypes and Virulence Potential of Shiga Toxin-Producing Escherichia coli. Appl Environ Microbiol 80: 1411-1420. doi:10.1128/AEM.03018-13.
12. Grissa I, Vergnaud G, Pourcel C (2007) CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35: W52-7. doi:10.1093/nar/gkm360.
13. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402. doi:10.1093/nar/25.17.3389. (Pubitemid 27359211)
14. Semenova E, Jore MM, Datsenko KA, Semenova A, Westra ER, et al. (2011) Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc Natl Acad Sci U S A 108: 10098-10103. doi:10.1073/pnas.1104144108.
15. Esvelt KM, Mali P, Braff JL, Moosburner M, Yaung SJ, et al. (2013) Orthogonal Cas9 proteins for RNA-guided gene regulation and editing. Nat Methods 10: 1116-1121. doi:10.1038/nmeth.2681.
16. Georgopoulos CP (1967) Isolation and preliminary characterization of T4 mutants with nonglucosylated DNA. Biochem Biophys Res Commun 28: 179-184. doi:http://dx.doi.org/10.1016/0006-291X(67)90426-3.
17. Warren RAJ (1980) Modified bases in bacteriophage DNAs. Annu Rev Microbiol 34: 137-158. doi:10.1146/annurev.mi.34.100180.001033.
18. Petrov VM, Ratnayaka S, Nolan JM, Miller ES, Karam JD (2010) Genomes of the T4-related bacteriophages as windows on microbial genome evolution. Virol J 7: 292. doi:10.1186/1743-422X-7-292.
19. Dupuis M-È, Villion M, Magadán AH, Moineau S (2013) CRISPR-Cas and restriction-modification systems are compatible and increase phage resistance. Nat Commun 4: 2087. doi:10.1038/ncomms3087.
20. Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, et al. (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31: 827-832. doi:10.1038/nbt.2647.
21. Monod C, Repoila F, Kutateladze M, Tétart F, Krisch HM (1997) The genome of the pseudo T-even bacteriophages, a diverse group that resembles T4. J Mol Biol 267: 237-249. doi:10.1006/jmbi.1996.0867. (Pubitemid 27149837)
22. Snyder L, Gold L, Kutter E (1976) A gene of bacteriophage T4 whose product prevents true late transcription on cytosine-containing T4 DNA. Proc Natl Acad Sci U S A 73: 3098-3102.
23. Kornberg S, Zimmerman S, Kornberg A (1961) Glucosylation of deoxyribonucleic acid by enzymes from bacteriophage-infected Escherichia coli. J Biol Chem 236: 1487-1493.
24. Choo Y (1998) Recognition of DMA methylation by zinc fingers. Nat Struct Biol 5: 264-265. doi:10.1038/nsb0498-264.
25. Valton J, Dupuy A, Daboussi F, Thomas S, Maréchal A, et al. (2012) Overcoming transcription activator-like effector (TALE) DNA binding domain sensitivity to cytosine methylation. J Biol Chem 287: 38427-38432. doi:10.1074/jbc.C112.408864.
26. Fineran PC, Gerritzen MJH, Suárez-Diez M, Künne T, Boekhorst J, et al. (2014) Degenerate target sites mediate rapid primed CRISPR adaptation. Proc Natl Acad Sci U S A. Available: http://www.ncbi.nlm.nih.gov/pubmed/ 24711427. Accessed 9 April 2014.
27. Deveau H, Barrangou R, Garneau JE, Labonté J, Fremaux C, et al. (2008) Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J Bacteriol 190: 1390-1400. doi:10.1128/JB.01412-07. (Pubitemid 351215022)
28. Levin BR, Moineau S, Bushman M, Barrangou R (2013) The population and evolutionary dynamics of phage and bacteria with CRISPR-mediated immunity. PLoS Genet 9: e1003312. doi:10.1371/journal.pgen.1003312.
29. Magadán AH, Dupuis M-È, Villion M, Moineau S (2012) Cleavage of phage DNA by the Streptococcus thermophilus CRISPR3-Cas system. PLoS One 7: e40913. doi:10.1371/journal.pone.0040913.
30. Garneau JE, Dupuis M-È, Villion M, Romero DA, Barrangou R, et al. (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468: 67-71. doi:10.1038/nature09523.
31. Bondy-Denomy J, Pawluk A, Maxwell KL, Davidson AR (2013) Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 493: 429-432. doi:10.1038/nature11723.
32. Seed KD, Lazinski DW, Calderwood SB, Camilli A (2013) A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 494: 489-491. doi:10.1038/nature11927.
33. Sheludchenko MS, Huygens F, Hargreaves MH (2010) Highly discriminatory single-nucleotide polymorphism interrogation of Escherichia coli by use of allele-specific real-time PCR and eBURST analysis. Appl Environ Microbiol 76: 4337-4345. doi:10.1128/AEM.00128-10.