Bacteriophage resistance mechanisms (original) (raw)

• Brüssow, H. & Hendrix, R. W. Phage genomics: small is beautiful. Cell 108, 13–16 (2002).
  Article PubMed Google Scholar
• Okafor, N. Modern Industrial Microbiology and Biotechnology (Science Publishers, Enfield, New Hampshire, 2007).
  Google Scholar
• Hutkins, R. W. Microbiology and Technology of Fermented Foods (Blackwell Publishing, Chicago, 2006).
  Book Google Scholar
• Émond, É. & Moineau, S. in Bacteriohpage: Genetics and Molecular Biology (eds McGrath, S. & Van Sinderen, D.) 93–123 (Caister Academic, Norwich, Norfolk, 2007).
  Google Scholar
• Sturino, J. M. & Klaenhammer, T. R. Engineered bacteriophage-defence systems in bioprocessing. Nature Rev. Microbiol. 4, 395–404 (2006).
  Article CAS Google Scholar
• O'Flaherty, S., Ross, R. P. & Coffey, A. Bacteriophage and their lysins for elimination of infectious bacteria. FEMS Microbiol. Rev. 33, 801–819 (2009).
  Article CAS PubMed Google Scholar
• Mattey, M. & Spencer, J. Bacteriophage therapy — cooked goose or Phoenix rising? Curr. Opin. Biotechnol. 19, 608–612 (2008).
  Article CAS PubMed Google Scholar
• Hanlon, G. W. Bacteriophages: an appraisal of their role in the treatment of bacterial infections. Int. J. Antimicrobi. Agents 30, 118–128 (2007).
  Article CAS Google Scholar
• Campbell, A. The future of bacteriophage biology. Nature Rev. Genet. 4, 471–477 (2003).
  Article CAS PubMed Google Scholar
• Sulakvelidze, A., Alavidze, Z. & Morris, J. G. Jr. Bacteriophage therapy. Antimicrob. Agents Chemother. 45, 649–659 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Foster, T. J. Immune evasion by staphylococci. Nature Rev. Microbiol. 3, 948–958 (2005).
  Article CAS Google Scholar
• Nordström, K. & Forsgren, A. Effect of protein A on adsorption of bacteriophages to Staphylococcus aureus. J. Virol. 14, 198–202 (1974).
  PubMed PubMed Central Google Scholar
• Pedruzzi, I., Rosenbusch, J. P. & Locher, K. P. Inactivation in vitro of the Escherichia coli outer membrane protein FhuA by a phage T5-encoded lipoprotein. FEMS Microbiol. Lett. 168, 119–125 (1998).
  Article CAS PubMed Google Scholar
• Riede, I. & Eschbach, M. L. Evidence that TraT interacts with OmpA of Escherichia coli. FEBS Lett. 205, 241–245 (1986).
  Article CAS PubMed Google Scholar
• Uhl, M. A. & Miller, J. F. Integration of multiple domains in a two-component sensor protein: the Bordetella pertussis BVgAS phosphorelay. EMBO J. 15, 1028–1036 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Beier, D. & Gross, R. in Bacterial Signal Transduction: Networks and Drug Targets. (ed. Utsumi, R.) 149–160 (Springer, New York, 2008).
  Book Google Scholar
• Liu, M. et al. Reverse transcriptase-mediated tropism switching in Bordetella bacteriophage. Science 295, 2091–2094 (2002). This fascinating paper describes how phages infecting Bordetella spp. can adapt to the cell surface variations that occur in their hosts in different environmental conditions.
  Article CAS PubMed Google Scholar
• Doulatov, S. et al. Tropism switching in Bordetella bacteriophage defines a family of diversity-generating retroelements. Nature 431, 476–481 (2004).
  Article CAS PubMed Google Scholar
• Medhekar, B. & Miller, J. F. Diversity-generating retroelements. Curr. Opin. Microbiol. 10, 388–395 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Ventura, M. et al. Prophage-like elements in bifidobacteria: insights from genomics, transcription, integration, distribution, and phylogenetic analysis. Appl. Environ. Microbiol. 71, 8692–8705 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Stummeyer, K. et al. Evolution of bacteriophages infecting encapsulated bacteria: lessons from Escherichia coli K1-specific phages. Mol. Microbiol. 60, 1123–1135 (2006).
  Article CAS PubMed Google Scholar
• Sutherland, I. W. Polysaccharide lyases. FEMS Microbiol. Rev. 16, 323–347 (1995). This is the most complete review on the topic of the enzymes that degrade polysaccharides.
  Article CAS PubMed Google Scholar
• Sutherland, I. W. Polysaccharases for microbial exopolysaccharides. Carbohydr. Polym. 38, 319–328 (1999).
  Article CAS Google Scholar
• Sutherland, I. W., Hughes, K. A., Skillman, L. C. & Tait, K. The interaction of phage and biofilms. FEMS Microbiol. Lett. 232, 1–6 (2004).
  Article CAS PubMed Google Scholar
• Linhardt, R. J., Galliher, P. M. & Cooney, C. L. Polyccharide lyases. Appl. Biochem. Biotechnol. 12, 135–176 (1986).
  Article CAS PubMed Google Scholar
• Hammad, A. M. M. Evaluation of alginate-encapsulated Azotobacter chroococcum as a phage-resistant and an effective inoculum. J. Basic Microbiol. 38, 9–16 (1998).
  Article CAS Google Scholar
• Hanlon, G. W., Denyer, S. P., Olliff, C. J. & Ibrahim, L. J. Reduction in exopolysaccharide viscosity as an aid to bacteriophage penetration through Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 67, 2746–2753 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Castillo, F. J. & Bartell, P. F. Studies on bacteriophage-2 receptors of Pseudomonas aeruginosa. J. Virol. 14, 904–909 (1974).
  CAS PubMed PubMed Central Google Scholar
• Castillo, F. J. & Bartell, P. F. Localization and functional role of Pseudomonas bacteriophage 2 depolymerase. J. Virol. 18, 701–708 (1976).
  CAS PubMed PubMed Central Google Scholar
• Temple, G. S., Ayling, P. D. & Wilkinson, S. G. Isolation and characterization of a lipopolysaccharide-specific bacteriophage of Pseudomonas aeruginosa. Microbios 45, 81–91 (1986).
  CAS PubMed Google Scholar
• Hynes, W. L., Hancock, L. & Ferretti, J. J. Analysis of a 2nd bacteriophage hyaluronidase gene from Streptococcus pyogenes: evidence for a 3rd hyaluronidase involved in extracellular enzymatic activity. Infect. Immun. 63, 3015–3020 (1995).
  CAS PubMed PubMed Central Google Scholar
• Boulnois, G. J. & Roberts, I. S. Genetics of capsular polysaccharide production in bacteria. Curr. Top. Microbiol. Immunol. 150, 1–18 (1990).
  CAS PubMed Google Scholar
• Moses, A. E. et al. Relative contributions of hyaluronic acid capsule and M protein to virulence in a mucoid strain of the group A Streptococcus. Infect. Immun. 65, 64–71 (1997).
  CAS PubMed PubMed Central Google Scholar
• McClean, D. The capsulation of streptococci and its relation to diffusion factor (hyaluronidase). J. Pathol. Bacteriol. 53, 13–27 (1941).
  Article CAS Google Scholar
• Kjems, E. Studies on streptococcal bacteriophages. I. Technique of isolating phage-producing strains. Acta Pathol. Microbiol. Scand. 36, 433–440 (1955).
  Article CAS PubMed Google Scholar
• Benchetrit, L. C., Gray, E. D. & Wannamaker, L. W. Hyaluronidase activity of bacteriophages of group A streptococci. Infect. Immun. 15, 527–532 (1977).
  CAS PubMed PubMed Central Google Scholar
• Stirm, S. Escherichia coli K bacteriophages, I. Isolation and introductory characterization of five Escherichia coli K bacteriophages. J. Virol. 2, 1107–1114 (1968).
  CAS PubMed PubMed Central Google Scholar
• Steinbacher, S., Miller, S., Baxa, U., Weintraub, A. & Seckler, R. Interaction of Salmonella phage P22 with its O-antigen receptor studied by X-ray crystallography. J. Biol. Chem. 378, 337–343 (1997).
  CAS Google Scholar
• Perry, L. L. et al. Sequence analysis of Escherichia coli O157:H7 bacteriophage ΦV10 and identification of a phage-encoded immunity protein that modifies the O157 antigen. FEMS Microbiol. Lett. 292, 182–186 (2009).
  Article CAS PubMed Google Scholar
• Zaleski, P., Wojciechowski, M. & Piekarowicz, A. The role of Dam methylation in phase variation of Haemophilus influenzae genes involved in defence against phage infection. Microbiology 151, 3361–3369 (2005).
  Article CAS PubMed Google Scholar
• Destoumieux-Garzon, D. et al. The iron-siderophore transporter FhuA is the receptor for the antimicrobial peptide microcin J25: role of the microcin Val11-Pro16 β-hairpin region in the recognition mechanism. Biochem. J. 389, 869–876 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Lu, M. J., Stierhof, Y. D. & Henning, U. Location and unusual membrane topology of the immunity protein of the Escherichia coli phage T4. J. Virol. 67, 4905–4913 (1993).
  CAS PubMed PubMed Central Google Scholar
• Lu, M. J. & Henning, U. Superinfection exclusion by T-even-type coliphages. Trends Microbiol. 2, 137–139 (1994). This paper describes the superinfection exclusion mechanisms that are found in phage T4.
  Article CAS PubMed Google Scholar
• Moak, M. & Molineux, I. J. Role of the Gp16 lytic transglycosylase motif in bacteriophage T7 virions at the initiation of infection. Mol. Microbiol. 37, 345–355 (2000).
  Article CAS PubMed Google Scholar
• Kliem, M. & Dreiseikelmann, B. The superimmunity gene sim of bacteriophage P1 causes superinfection exclusion. Virology 171, 350–355 (1989).
  Article CAS PubMed Google Scholar
• Maillou, J. & Dreiseikelmann, B. The sim gene of Escherichia coli phage P1: nucleotide sequence and purification of the processed protein. Virology 175, 500–507 (1990).
  Article CAS PubMed Google Scholar
• Hofer, B., Ruge, M. & Dreiseikelmann, B. The superinfection exclusion gene (sieA) of bacteriophage P22: identification and overexpression of the gene and localization of the gene product. J. Bacteriol. 177, 3080–3086 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Garvey, P., Hill, C. & Fitzgerald, G. The lactococcal plasmid pNP40 encodes a third bacteriophage resistance mechanism, one which affects phage DNA penetration. Appl. Environ. Microbiol. 62, 676–679 (1996).
  CAS PubMed PubMed Central Google Scholar
• Akçelik, M. A phage DNA injection-blocking type resistance mechanism encoded by chromosomal DNA in Lactococcus lactis subsp. lactis PLM-18. Milchwissenschaft 53, 619–622 (1998).
  Google Scholar
• McGrath, S., Fitzgerald, G. F. & van Sinderen, D. Identification and characterization of phage-resistance genes in temperate lactococcal bacteriophages. Mol. Microbiol. 43, 509–520 (2002).
  Article CAS PubMed Google Scholar
• Mahony, J., McGrath, S., Fitzgerald, G. F. & van Sinderen, D. Identification and characterization of lactococcal-prophage-carried superinfection exclusion genes. Appl. Environ. Microbiol. 74, 6206–6215 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Sun, X., Gohler, A., Heller, K. J. & Neve, H. The ltp gene of temperate Streptococcus thermophilus phage TP-J34 confers superinfection exclusion to Streptococcus thermophilus and Lactococcus lactis. Virology 350, 146–157 (2006).
  Article CAS PubMed Google Scholar
• Pingoud, A., Fuxreiter, M., Pingoud, V. & Wende, W. Type II restriction endonucleases: structure and mechanism. Cell. Mol. Life Sci. 62, 685–707 (2005).
  Article CAS PubMed Google Scholar
• Pingoud, A. M. Restriction Endonucleases (Springer, Berlin, 2004).
  Book Google Scholar
• Kruger, D. H. & Bickle, T. A. Bacteriophage survival: multiple mechanisms for avoiding the deoxyribonucleic-acid restriction systems of their hosts. Microbiol. Rev. 47, 345–360 (1983).
  CAS PubMed PubMed Central Google Scholar
• Kruger, D. H., Barcak, G. J. & Smith, H. O. Abolition of DNA recognition site resistance to the restriction endonuclease _Eco_RII. Biomed. Biochim. Acta 47, K1–K5 (1988).
  CAS PubMed Google Scholar
• Tock, M. R. & Dryden, D. T. The biology of restriction and anti-restriction. Curr. Opin. Microbiol. 8, 466–472 (2005).
  Article CAS PubMed Google Scholar
• Wilson, G. G. & Murray, N. E. Restriction and modification systems. Annu. Rev. Genet. 25, 585–627 (1991).
  Article CAS PubMed Google Scholar
• McGrath, S., Seegers, J. F. M. L., Fitzgerald, G. F. & van Sinderen, D. Molecular characterization of a phage-encoded resistance system in Lactococcus lactis. Appl. Environ. Microbiol. 65, 1891–1899 (1999).
  CAS PubMed PubMed Central Google Scholar
• Bickle, T. A. & Kruger, D. H. Biology of DNA restriction. Microbiol. Rev. 57, 434–450 (1993).
  CAS PubMed PubMed Central Google Scholar
• Vovis, G. F. & Lacks, S. Complementary action of restriction enzymes endo R-_Dpn_I and endo R-_Dpn_II on bacteriophage-f1 DNA. J. Mol. Biol. 115, 525–538 (1977).
  Article CAS PubMed Google Scholar
• Raleigh, E. A. & Wilson, G. Escherichia coli K-12 restricts DNA containing 5-methylcytosine. Proc. Natl Acad. Sci. USA 83, 9070–9074 (1986).
  Article CAS PubMed PubMed Central Google Scholar
• Bair, C. L. & Black, L. W. A type IV modification dependent restriction nuclease that targets glucosylated hydroxymethyl cytosine modified DNAs. J. Mol. Biol. 366, 768–778 (2007). This article describes how phage T4 subverts the GmrS–GmrD system (which specifically cleaves glucosyl-hydroxymethylcytosine-modified DNA) using an injected protein inhibitor.
  Article CAS PubMed Google Scholar
• Bair, C. L., Rifat, D. & Black, L. W. Exclusion of glucosyl-hydroxymethylcytosine DNA containing bacteriophages is overcome by the injected protein inhibitor IPI*. J. Mol. Biol. 366, 779–789 (2007).
  Article CAS PubMed Google Scholar
• Rifat, D., Wright, N. T., Varney, K. M., Weber, D. J. & Black, L. W. Restriction endonuclease inhibitor IPI* of bacteriophage T4: a novel structure for a dedicated target. J. Mol. Biol. 375, 720–734 (2008).
  Article CAS PubMed Google Scholar
• Zabeau, M., Friedman, S., Montagu, M. V. & Schell, J. The ral gene of phage λ.1. Identification of a non-essential gene that modulates restriction and modification in Escherichia coli. Mol. Gen. Genet. 179, 63–73 (1980).
  Article CAS PubMed Google Scholar
• Zissler, J., Singer, E. R. & Schaefer, F. in The Bacteriophage λ (ed. Hershey, A. D.) 455–475 (Cold Spring Harbor Laboratory Press, New York, 1971).
  Google Scholar
• King, G. & Murray, N. E. Restriction alleviation and modification enhancement by the Rac prophage of Escherichia coli K-12. Mol. Microbiol. 16, 769–777 (1995).
  Article CAS PubMed Google Scholar
• Toothman, P. Restriction alleviation by bacteriophages lambda and lambda reverse. J. Virol. 38, 621–631 (1981).
  CAS PubMed PubMed Central Google Scholar
• Walkinshaw, M. D. et al. Structure of Ocr from bacteriophage T7, a protein that mimics B-form DNA. Mol. Cell 9, 187–194 (2002).
  Article CAS PubMed Google Scholar
• Studier, F. W. Analysis of bacteriophage T7 early RNAs and proteins on slab gels. J. Mol. Biol. 79, 237–248 (1973).
  Article CAS PubMed Google Scholar
• Atanasiu, C., Su, T. J., Sturrock, S. S. & Dryden, D. T. Interaction of the ocr gene 0.3 protein of bacteriophage T7 with _Eco_KI restriction/modification enzyme. Nucleic Acids Res. 30, 3936–3944 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Bandyopadhyay, P. K., Studier, F. W., Hamilton, D. L. & Yuan, R. Inhibition of the type I restriction-modification enzymes _Eco_B and _Eco_K by the gene 0.3 protein of bacteriophage T7. J. Mol. Biol. 182, 567–578 (1985).
  Article CAS PubMed Google Scholar
• Kennaway, C. K. et al. The structure of M.EcoKI type I DNA methyltransferase with a DNA mimic antirestriction protein. Nucleic Acids Res. 37, 762–770 (2009).
  Article CAS PubMed Google Scholar
• Studier, F. W. & Movva, N. R. SAMase gene of bacteriophage T3 is responsible for overcoming host restriction. J. Virol. 19, 136–145 (1976).
  CAS PubMed PubMed Central Google Scholar
• Sistla, S. & Rao, D. N. _S_-Adenosyl-L-methionine-dependent restriction enzymes. Crit. Rev. Biochem. Mol. Biol. 39, 1–19 (2004).
  Article CAS PubMed Google Scholar
• Iida, S., Streiff, M. B., Bickle, T. A. & Arber, W. Two DNA antirestriction systems of bacteriophage P1, darA, and darB: characterization of darA − phage. Virology 157, 156–166 (1987).
  Article CAS PubMed Google Scholar
• Barrangou, R. et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315, 1709–1712 (2007). The first evidence that the CRISPR–Cas system is an immunity system against foreign DNA.
  Article CAS PubMed Google Scholar
• Sorek, R., Kunin, V. & Hugenholtz, P. CRISPR — a widespread system that provides acquired resistance against phages in bacteria and archaea. Nature Rev. Microbiol. 6, 181–186 (2008).
  Article CAS Google Scholar
• Marraffini, L. A. & Sontheimer, E. J. Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature 463, 568–571 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Marraffini, L. A. & Sontheimer, E. J. CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nature Rev. Genet. 11, 181–190 (2010).
  Article CAS PubMed Google Scholar
• Karginov, F. V. & Hannon, G. J. The CRISPR system: small RNA-guided defense in bacteria and archaea. Mol. Cell 37, 7–19 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Horvath, P. & Barrangou, R. CRISPR/Cas, the immune system of bacteria and archaea. Science 327, 167–170 (2010).
  Article CAS PubMed Google Scholar
• Ishino, Y., Shinagawa, H., Makino, K., Amemura, M. & Nakata, A. Nucleotide-sequence of the iap gene, responsible for alkaline-phosphatase isozyme conversion in Escherichia coli, and identification of the gene-product. J. Bacteriol. 169, 5429–5433 (1987).
  Article CAS PubMed PubMed Central Google Scholar
• Godde, J. S. & Bickerton, A. The repetitive DNA elements called CRISPRs and their associated genes: evidence of horizontal transfer among prokaryotes. J. Mol. Evol. 62, 718–729 (2006).
  Article CAS PubMed Google Scholar
• Horvath, P. et al. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J. Bacteriol. 190, 1401–1412 (2008).
  Article CAS PubMed Google Scholar
• Jansen, R., van Embden, J. D. A., Gaastra, W. & Schouls, L. M. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43, 1565–1575 (2002).
  Article CAS PubMed Google Scholar
• Makarova, K. S., Grishin, N. V., Shabalina, S. A., Wolf, Y. I. & Koonin, E. V. A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol. Direct 1, 7 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Vestergaard, G. et al. Stygiolobus rod-shaped virus and the interplay of crenarchaeal rudiviruses with the CRISPR antiviral system. J. Bacteriol. 190, 6837–6845 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Bolotin, A., Ouinquis, B., Sorokin, A. & Ehrlich, S. D. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151, 2551–2561 (2005).
  Article CAS PubMed Google Scholar
• Haft, D. H., Selengut, J., Mongodin, E. F. & Nelson, K. E. A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput. Biol. 1, 474–483 (2005).
  Article CAS Google Scholar
• Mojica, F. J. M., Diez-Villasenor, C., Garcia-Martinez, J. & Soria, E. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60, 174–182 (2005).
  Article CAS PubMed Google Scholar
• Pourcel, C., Salvignol, G. & Vergnaud, G. CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 151, 653–663 (2005).
  Article CAS PubMed Google Scholar
• Marraffini, L. A. & Sontheimer, E. J. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322, 1843–1845 (2008). This study shows that the CRISPR–Cas system targets foreign DNA.
  Article CAS PubMed PubMed Central Google Scholar
• Zegans, M. E. et al. Interaction between bacteriophage DMS3 and host CRISPR region inhibits group behaviors of P. aeruginosa. J. Bacteriol. 191, 210–219 (2009).
  Article CAS PubMed Google Scholar
• Mojica, F. J. M., Diez-Villasenor, C., Garcia-Martinez, J. & Almendros, C. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 155, 733–740 (2009).
  Article CAS PubMed Google Scholar
• Brouns, S. J. J. et al. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321, 960–964 (2008). A demonstration that one of the cas genes encodes an RNA endonuclease that is required for the CRISPR–Cas system to be active against phages.
  Article CAS PubMed PubMed Central Google Scholar
• Tang, T. H. et al. Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus. Proc. Natl Acad. Sci. USA 99, 7536–7541 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Tang, T. H. et al. Identification of novel non-coding RNAs as potential antisense regulators in the archaeon Sulfolobus solfataricus. Mol. Microbiol. 55, 469–481 (2005).
  Article CAS PubMed Google Scholar
• Deveau, H. et al. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol. 190, 1390–1400 (2008).
  Article CAS PubMed Google Scholar
• Andersson, A. F. & Banfield, J. F. Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320, 1047–1050 (2008).
  Article CAS PubMed Google Scholar
• Molineux, I. J. Host-parasite interactions: recent developments in the genetics of abortive phage infections. New Biol. 3, 230–236 (1991). A comprehensive review of the phage exclusion systems in E. coli.
  CAS PubMed Google Scholar
• Snyder, L. Phage-exclusion enzymes: a bonanza of biochemical and cell biology reagents? Mol. Microbiol. 15, 415–420 (1995). A summary of the progress that has been made in understanding the modes of action of phage exclusion systems in Gram-negative bacteria.
  Article CAS PubMed Google Scholar
• Parma, D. H. et al. The Rex system of bacteriophage lambda: tolerance and altruistic cell death. Genes Dev. 6, 497–510 (1992).
  Article CAS PubMed Google Scholar
• Snyder, L. & McWilliams, K. The rex genes of bacteriophage lambda can inhibit cell function without phage superinfection. Gene 81, 17–24 (1989).
  Article CAS PubMed Google Scholar
• Hinton, D. M. et al. Transcriptional takeover by σ appropriation: remodelling of the σ70 subunit of Escherichia coli RNA polymerase by the bacteriophage T4 activator MotA and co-activator AsiA. Microbiology 151, 1729–1740 (2005).
  Article CAS PubMed Google Scholar
• Kaufmann, G. Anticodon nucleases. Trends Biochem. Sci. 25, 70–74 (2000).
  Article CAS PubMed Google Scholar
• Bingham, R., Ekunwe, S. I. N., Falk, S., Snyder, L. & Kleanthous, C. The major head protein of bacteriophage T4 binds specifically to elongation factor Tu. J. Biol. Chem. 275, 23219–23226 (2000).
  Article CAS PubMed Google Scholar
• Cheng, X., Wang, W. & Molineux, I. J. F exclusion of bacteriophage T7 occurs at the cell membrane. Virology 326, 340–352 (2004).
  Article CAS PubMed Google Scholar
• Garcia, L. R. & Molineux, I. J. Incomplete entry of bacteriophage T7 DNA into F-plasmid containing Escherichia coli. J. Bacteriol. 177, 4077–4083 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Schmitt, C. K., Kemp, P. & Molineux, I. J. Genes 1.2 and 10 of bacteriophages T3 and T7 determine the permeability lesions observed in infected cells of Escherichia coli expressing the F plasmid gene pifA. J. Bacteriol. 173, 6507–6514 (1991).
  Article CAS PubMed PubMed Central Google Scholar
• Chopin, M.-C., Chopin, A. & Bidnenko, E. Phage abortive infection in lactococci: variations on a theme. Curr. Opin. Microbiol. 8, 473–479 (2005). This article is the most complete review on Abi mechanism in L. lactis.
  Article CAS PubMed Google Scholar
• Hill, C., Miller, L. A. & Klaenhammer, T. R. Nucleotide sequence and distribution of the pTR2030 resistance determinant (hsp) which aborts bacteriophage infection in lactococci. Appl. Environ. Microbiol. 56, 2255–2258 (1990).
  CAS PubMed PubMed Central Google Scholar
• Garvey, P., Fitzgerald, G. F. & Hill, C. Cloning and DNA sequence analysis of two abortive infection phage resistance determinants from the lactococcal plasmid pNP40. Appl. Environ. Microbiol. 61, 4321–4328 (1995).
  CAS PubMed PubMed Central Google Scholar
• Émond, É. et al. Phenotypic and genetic characterization of the bacteriophage abortive infection mechanism AbiK from Lactococcus lactis. Appl. Environ. Microbiol. 63, 1274–1283 (1997).
  PubMed PubMed Central Google Scholar
• Domingues, S., Chopin, A., Ehrlich, S. D. & Chopin, M.-C. The lactococcal abortive phage infection system AbiP prevents both phage DNA replication and temporal transcription switch. J. Bacteriol. 186, 713–721 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Bouchard, J. D., Dion, É., Bissonnette, F. & Moineau, Characterization of the two-component abortive phage infection mechanism AbiT from Lactococcus lactis. J. Bacteriol. 184, 6325–6332 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Dai, G. et al. Molecular characterization of a new abortive infection system (AbiU) from Lactococcus lactis LL51–51 Appl. Environ. Microbiol. 67, 5225–5232 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Cluzel, P. J., Chopin, A., Ehrlich, S. D. & Chopin, M.-C. Phage abortive infection mechanism from Lactococcus lactis subsp. lactis, expression of which is mediated by an Iso-ISS1 element. Appl. Environ. Microbiol. 57, 3547–3551 (1991).
  CAS PubMed PubMed Central Google Scholar
• O'Connor, L., Tangney, M. & Fitzgerald, G. F. Expression, regulation, and mode of action of the AbiG abortive infection system of Lactococcus lactis subsp. cremoris UC653. Appl. Environ. Microbiol. 65, 330–335 (1999).
  CAS PubMed PubMed Central Google Scholar
• Durmaz, E., Higgins, D. L. & Klaenhammer, T. R. Molecular characterization of a second abortive phage resistance gene present in Lactococcus lactis subsp. lactis ME2. J. Bacteriol. 174, 7463–7469 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• Émond, É. et al. AbiQ, an abortive infection mechanism from Lactococcus lactis. Appl. Environ. Microbiol. 64, 4748–4756 (1998).
  PubMed PubMed Central Google Scholar
• Bidnenko, E., Ehrlich, S. D. & Chopin, M.-C. Lactococcus lactis phage operon coding for an endonuclease homologous to RuvC. Mol. Microbiol. 28, 823–834 (1998).
  Article CAS PubMed Google Scholar
• Durmaz, E. & Klaenhammer, T. R. Abortive phage resistance mechanism AbiZ speeds the lysis clock to cause premature lysis of phage-infected Lactococcus lactis. J. Bacteriol. 189, 1417–1425 (2007).
  Article CAS PubMed Google Scholar
• Domingues, S., Chopin, A., Ehrlich, S. D. & Chopin, M.-C. A phage protein confers resistance to the lactococcal abortive infection mechanism AbiP. J. Bacteriol. 186, 3278–3281 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Domingues, S. et al. The lactococcal abortive infection protein AbiP is membrane-anchored and binds nucleic acids. Virology 373, 14–24 (2008).
  Article CAS PubMed Google Scholar
• Boucher, I., Émond, É., Dion, É., Montpetit, D. & Moineau, S. Microbiological and molecular impacts of AbiK on the lytic cycle of Lactococcus lactis phages of the 936 and P335 species. Microbiology 146, 445–453 (2000).
  Article CAS PubMed Google Scholar
• Bouchard, J. D. & Moineau, S. Lactococcal phage genes involved in sensitivity to AbiK and their relation to single-strand annealing proteins. J. Bacteriol. 186, 3649–3652 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Fortier, L.-C., Bouchard, J. D. & Moineau, S. Expression and site-directed mutagenesis of the lactococcal abortive phage infection protein AbiK. J. Bacteriol. 187, 3721–3730 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Fineran, P. C. et al. The phage abortive infection system, ToxIN, functions as a protein–RNA toxin–antitoxin pair. Proc. Natl Acad. Sci. USA 106, 894–899 (2009). The research described in this paper is the most valuable study on the use of TA systems as antiphage mechanisms.
  Article CAS PubMed PubMed Central Google Scholar
• Magnuson, R. D. Hypothetical functions of toxin-antitoxin systems. J. Bacteriol. 189, 6089–6092 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Blower, T. R. et al. Mutagenesis and functional characterisation of the RNA and protein components of the toxIN abortive infection and toxin-antitoxin locus of Erwinia. J. Bacteriol. 191, 6029–6039 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Pecota, D. C. & Wood, T. K. Exclusion of T4 phage by the hok/sok killer locus from plasmid R1. J. Bacteriol. 178, 2044–2050 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Hazan, R. & Engelberg-Kulka, H. _Escherichia coli mazEF_-mediated cell death as a defense mechanism that inhibits the spread of phage P1. Mol. Genet. Genomics 272, 227–234 (2004).
  Article CAS PubMed Google Scholar
• Norrby, E. Nobel Prizes and the emerging virus concept. Arch. Virol. 153, 1109–1123 (2008).
  Article CAS PubMed Google Scholar