Innate and adaptive immunity in bacteria: Mechanisms of programmed genetic variation to fight bacteriophages

Current Opinion in Immunology

Volumn 24, Issue 1, 2012, Pages 15-20

  Bikard, David ^a   Marraffini, Luciano A ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; ADSORPTION; BACTERIAL CELL; BACTERIAL IMMUNITY; BACTERIOPHAGE; CELL SURVIVAL; EVOLUTION; GENE LOCUS; GENETIC VARIABILITY; INFECTION RESISTANCE; INNATE IMMUNITY; NONHUMAN; POINT MUTATION; PROKARYOTE; RETROPOSON; REVIEW;

ADAPTIVE IMMUNITY; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIOPHAGES; GENETIC VARIATION; IMMUNITY, INNATE;

EID: 84857041376     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2011.10.005     Document Type: Review

References (57)

1. Fuhrman J.A. Marine viruses and their biogeochemical and ecological effects. Nature 1999, 399:541-548.
2. Suttle C.A. Marine viruses-major players in the global ecosystem. Nat Rev Microbiol 2007, 5:801-812.
3. Mc Grath S., Fitzgerald G.F., van Sinderen D. Bacteriophages in dairy products: proscons. Biotechnol J 2007, 2:450-455.
4. Stern A., Sorek R. The phage-host arms race: shaping the evolution of microbes. Bioessays 2011, 33:43-51.
5. Hyman P., Abedon S.T. Bacteriophage host range and bacterial resistance. Adv Appl Microbiol 2010, 70:217-248.
6. Labrie S.J., Samson J.E., Moineau S. Bacteriophage resistance mechanisms. Nat Rev Microbiol 2010, 8:317-327.
7. Clement J.M., Lepouce E., Marchal C., Hofnung M. Genetic study of a membrane protein: DNA sequence alterations due to 17 lamB point mutations affecting adsorption of phage lambda. EMBO J 1983, 2:77-80.
8. Hofnung M., Jezierska A., Braun-Breton C. lamB mutations in E. coli K12: growth of lambda host range mutants and effect of nonsense suppressors. Mol Gen Genet 1976, 145:207-213.
9. Werts C., Michel V., Hofnung M., Charbit A. Adsorption of bacteriophage lambda on the LamB protein of Escherichia coli K-12: point mutations in gene J of lambda responsible for extended host range. J Bacteriol 1994, 176:941-947.
10. Drexler K., Riede I., Montag D., Eschbach M.L., Henning U. Receptor specificity of the Escherichia coli T-even type phage Ox2 mutational alterations in host range mutants. J Mol Biol 1989, 207:797-803.
11. Henderson I.R., Owen P., Nataro J.P. Molecular switches-the ON and OFF of bacterial phase variation. Mol Microbiol 1999, 33:919-932.
12. van der Woude M.W. Phase variation: how to create and coordinate population diversity. Curr Opin Microbiol 2011, 14:205-211.
13. Hood D.W., Deadman M.E., Jennings M.P., Bisercic M., Fleischmann R.D., Venter J.C., Moxon E.R. DNA repeats identify novel virulence genes in Haemophilus influenzae. Proc Natl Acad Sci U S A 1996, 93:11121-11125.
14. Bayliss C.D., Sweetman W.A., Moxon E.R. Mutations in Haemophilus influenzae mismatch repair genes increase mutation rates of dinucleotide repeat tracts but not dinucleotide repeat-driven pilin phase variation rates. J Bacteriol 2004, 186:2928-2935.
15. 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 2005, 151:3361-3369.
16. Samuel A.D., Pitta T.P., Ryu W.S., Danese P.N., Leung E.C., Berg H.C. Flagellar determinants of bacterial sensitivity to χ-phage. Proc Natl Acad Sci U S A 1999, 96:9863-9866.
17. Raimondo L.M., Lundh N.P., Martinez R.J. Primary adsorption site of phage PBS1: the flagellum of Bacillus subtilis. J Virol 1968, 2:256-264.
18. Valentine R.C., Strand M. Complexes of F-pili and RNA bacteriophage. Science 1965, 148:511-513.
19. Abraham J.M., Freitag C.S., Clements J.R., Eisenstein B.I. An invertible element of DNA controls phase variation of type 1 fimbriae of Escherichia coli. Proc Natl Acad Sci U S A 1985, 82:5724-5727.
20. Segal E., Billyard E., So M., Storzbach S., Meyer T.F. Role of chromosomal rearrangement in N. gonorrhoeae pilus phase variation. Cell 1985, 40:293-300.
21. Zieg J., Silverman M., Hilmen M., Simon M. Recombinational switch for gene expression. Science 1977, 196:170-172.
22. Ikeda J.S., Schmitt C.K., Darnell S.C., Watson P.R., Bispham J., Wallis T.S., Weinstein D.L., Metcalf E.S., Adams P., O'Connor C.D., et al. Flagellar phase variation of Salmonella enterica serovar Typhimurium contributes to virulence in the murine typhoid infection model but does not influence Salmonella-induced enteropathogenesis. Infect Immun 2001, 69:3021-3030.
23. Simon M., Zieg J., Silverman M., Mandel G., Doolittle R. Phase variation: evolution of a controlling element. Science 1980, 209:1370-1374.
24. Komano T. Shufflons: multiple inversion systems and integrons. Annu Rev Genet 1999, 33:171-191.
25. Komano T., Kubo A., Nisioka T. Shufflon: multi-inversion of four contiguous DNA segments of plasmid R64 creates seven different open reading frames. Nucleic Acids Res 1987, 15:1165-1172.
26. Komano T., Kim S.R., Yoshida T. Mating variation by DNA inversions of shufflon in plasmid R64. Adv Biophys 1995, 31:181-193.
27. Kamp D., Kahmann R., Zipser D., Broker T.R., Chow L.T. Inversion of the G DNA segment of phage Mu controls phage infectivity. Nature 1978, 271:577-580.
28. van de Putte P., Cramer S., Giphart-Gassler M. Invertible DNA determines host specificity of bacteriophage mu. Nature 1980, 286:218-222.
29. Sandmeier H., Iida S., Arber W. DNA inversion regions Min of plasmid p15B and Cin of bacteriophage P1: evolution of bacteriophage tail fiber genes. J Bacteriol 1992, 174:3936-3944.
30. Sandmeier H. Acquisition and rearrangement of sequence motifs in the evolution of bacteriophage tail fibres. Mol Microbiol 1994, 12:343-350.
31. Medhekar B., Miller J.F. Diversity-generating retroelements. Curr Opin Microbiol 2007, 10:388-395.
32. Dai W., Hodes A., Hui W.H., Gingery M., Miller J.F., Zhou Z.H. Three-dimensional structure of tropism-switching Bordetella bacteriophage. Proc Natl Acad Sci U S A 2010, 107:4347-4352.
33. Liu M., Deora R., Doulatov S.R., Gingery M., Eiserling F.A., Preston A., Maskell D.J., Simons R.W., Cotter P.A., Parkhill J., et al. Reverse transcriptase-mediated tropism switching in Bordetella bacteriophage. Science 2002, 295:2091-2094.
34. Simon D.M., Zimmerly S. A diversity of uncharacterized reverse transcriptases in bacteria. Nucleic Acids Res 2008, 36:7219-7229.
35. De Bolle X., Bayliss C.D., Field D., van de Ven T., Saunders N.J., Hood D.W., Moxon E.R. The length of a tetranucleotide repeat tract in Haemophilus influenzae determines the phase variation rate of a gene with homology to type III DNA methyltransferases. Mol Microbiol 2000, 35:211-222.
36. Bayliss C.D., Callaghan M.J., Moxon E.R. High allelic diversity in the methyltransferase gene of a phase variable type III restriction-modification system has implications for the fitness of Haemophilus influenzae. Nucleic Acids Res 2006, 34:4046-4059.
37. Ryan K.A., Lo R.Y. Characterization of a CACAG pentanucleotide repeat in Pasteurella haemolytica and its possible role in modulation of a novel type III restriction-modification system. Nucleic Acids Res 1999, 27:1505-1511.
38. de Vries N., Duinsbergen D., Kuipers E.J., Pot R.G., Wiesenekker P., Penn C.W., van Vliet A.H., Vandenbroucke-Grauls C.M., Kusters J.G. Transcriptional phase variation of a type III restriction-modification system in Helicobacter pylori. J Bacteriol 2002, 184:6615-6623.
39. Saunders N.J., Jeffries A.C., Peden J.F., Hood D.W., Tettelin H., Rappuoli R., Moxon E.R. Repeat-associated phase variable genes in the complete genome sequence of Neisseria meningitidis strain MC58. Mol Microbiol 2000, 37:207-215.
40. Srikhanta Y.N., Fox K.L., Jennings M.P. The phasevarion: phase variation of type III DNA methyltransferases controls coordinated switching in multiple genes. Nat Rev Microbiol 2010, 8:196-206.
41. Srikhanta Y.N., Maguire T.L., Stacey K.J., Grimmond S.M., Jennings M.P. The phasevarion: a genetic system controlling coordinated, random switching of expression of multiple genes. Proc Natl Acad Sci U S A 2005, 102:5547-5551.
42. Cerdeno-Tarraga A.M., Patrick S., Crossman L.C., Blakely G., Abratt V., Lennard N., Poxton I., Duerden B., Harris B., Quail M.A., et al. Extensive DNA inversions in the B. fragilis genome control variable gene expression. Science 2005, 307:1463-1465.
43. Deveau H., Garneau J.E., Moineau S. CRISPR/Cas system and its role in phage-bacteria interactions. Annu Rev Microbiol 2010, 64:475-493.
44. Horvath P., Barrangou R. CRISPR/Cas, the immune system of bacteria and archaea. Science 2010, 327:167-170.
45. Marraffini L.A., Sontheimer E.J. CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 2010, 11:181-190.
46. Brouns S.J., Jore M.M., Lundgren M., Westra E.R., Slijkhuis R.J., Snijders A.P., Dickman M.J., Makarova K.S., Koonin E.V., van der Oost J. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 2008, 321:960-964.
47. Carte J., Wang R., Li H., Terns R.M., Terns M.P. Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev 2008, 22:3489-3496.
48. Haurwitz R.E., Jinek M., Wiedenheft B., Zhou K., Doudna J.A. Sequence- and structure-specific RNA processing by a CRISPR endonuclease. Science 2010, 329:1355-1358.
49. Garneau J.E., Dupuis M.E., Villion M., Romero D.A., Barrangou R., Boyaval P., Fremaux C., Horvath P., Magadan A.H., Moineau S. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 2010, 468:67-71.
50. Hale C.R., Zhao P., Olson S., Duff M.O., Graveley B.R., Wells L., Terns R.M., Terns M.P. RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 2009, 139:945-956.
51. Marraffini L.A., Sontheimer E.J. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 2008, 322:1843-1845.
52. Marraffini L.A., Sontheimer E.J. Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature 2010, 463:568-571.
53. Barrangou R., Fremaux C., Deveau H., Richards M., Boyaval P., Moineau S., Romero D.A., Horvath P. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007, 315:1709-1712.
54. Deveau H., Barrangou R., Garneau J.E., Labonte J., Fremaux C., Boyaval P., Romero D.A., Horvath P., Moineau S. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J Bacteriol 2008, 190:1390-1400.
55. Pul U., Wurm R., Arslan Z., Geissen R., Hofmann N., Wagner R. Identification and characterization of E. coli CRISPR-cas promoters and their silencing by H-NS. Mol Microbiol 2010, 75:1495-1512.
56. Westra E.R., Pul U., Heidrich N., Jore M.M., Lundgren M., Stratmann T., Wurm R., Raine A., Mescher M., Van Heereveld L., et al. H-NS-mediated repression of CRISPR-based immunity in Escherichia coli K12 can be relieved by the transcription activator LeuO. Mol Microbiol 2010, 77:1380-1393.
57. Wiedenheft B., Zhou K., Jinek M., Coyle S.M., Ma W., Doudna J.A. Structural basis for DNase activity of a conserved protein implicated in CRISPR-mediated genome defense. Structure 2009, 17:904-912.