Adapting to new threats: The generation of memory by CRISPR-Cas immune systems

Molecular Microbiology

Volumn 93, Issue 1, 2014, Pages 1-9

  Heler, Robert ^a   Marraffini, Luciano A ^a   Bikard, David ^a,b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEASE;

ADAPTIVE IMMUNITY; BACTERIUM; CAS GENE; CELL PROTECTION; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DNA SEQUENCE; EVOLUTIONARY ADAPTATION; GENE; GENE INSERTION; GENE LOCUS; GENE STRUCTURE; GENE TARGETING; GENETIC ASSOCIATION; IMMUNE SYSTEM; IMMUNOLOGICAL MEMORY; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTOSPACER ADJACENT MOTIF; REVIEW; ADAPTATION; ARCHAEON; BACTERIA; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIOPHAGE; BIOLOGICAL MODEL; CRISPR CAS SYSTEM; GENETICS; GENOME; IMMUNOLOGY; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; ARCHAEA; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIOPHAGES; CRISPR-CAS SYSTEMS; GENOME; MODELS, GENETIC;

EID: 84903471734     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12640     Document Type: Review

References (68)

1. Agari, Y., Sakamoto, K., Tamakoshi, M., Oshima, T., Kuramitsu, S., and Shinkai, A. (2010) Transcription profile of Thermus thermophilus CRISPR systems after phage infection. J Mol Biol 395: 270-281.
2. Almendros, C., Guzman, N.M., Diez-Villasenor, C., Garcia-Martinez, J., and Mojica, F.J. (2012) Target motifs affecting natural immunity by a constitutive CRISPR-Cas system in Escherichia coli. PLoS ONE 7: e50797.
3. Andersson, A.F., and Banfield, J.F. (2008) Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320: 1047-1050.
4. Arslan, Z., Wurm, R., Brener, O., Ellinger, P., Nagel-Steger, L., Oesterhelt, F., etal. (2013) Double-strand DNA end-binding and sliding of the toroidal CRISPR-associated protein Csn2. Nucleic Acids Res 41: 6347-6359.
5. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., etal. (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315: 1709-1712.
6. Beloglazova, N., Brown, G., Zimmerman, M.D., Proudfoot, M., Makarova, K.S., Kudritska, M., etal. (2008) A novel family of sequence-specific endoribonucleases associated with the clustered regularly interspaced short palindromic repeats. J Biol Chem 283: 20361-20371.
7. Bikard, D., and Marraffini, L.A. (2012) Innate and adaptive immunity in bacteria: mechanisms of programmed genetic variation to fight bacteriophages. Curr Opin Immunol 24: 15-20.
8. Bikard, D., Hatoum-Aslan, A., Mucida, D., and Marraffini, L.A. (2012) CRISPR interference can prevent natural transformation and virulence acquisition during in vivo bacterial infection. Cell Host Microbe 12: 177-186.
9. Bolotin, A., Quinquis, B., Sorokin, A., and Ehrlich, S.D. (2005) Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151: 2551-2561.
10. Brouns, S.J., Jore, M.M., Lundgren, M., Westra, E.R., Slijkhuis, R.J., Snijders, A.P., etal. (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321: 960-964.
11. Cady, K.C., Bondy-Denomy, J., Heussler, G.E., Davidson, A.R., and O'Toole, G.A. (2012) The CRISPR/Cas Adaptive Immune System of Pseudomonas aeruginosa Mediates Resistance to Naturally Occurring and Engineered Phages. J Bacteriol 194: 5728-5738.
12. Datsenko, K.A., Pougach, K., Tikhonov, A., Wanner, B.L., Severinov, K., and Semenova, E. (2012) Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system. Nat Commun 3: 945.
13. Deltcheva, E., Chylinski, K., Sharma, C.M., Gonzales, K., Chao, Y., Pirzada, Z.A., etal. (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471: 602-607.
14. Deveau, H., Barrangou, R., Garneau, J.E., Labonte, J., Fremaux, C., Boyaval, P., etal. (2008) Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J Bacteriol 190: 1390-1400.
15. Diez-Villasenor, C., Guzman, N.M., Almendros, C., Garcia-Martinez, J., and Mojica, F.J. (2013) CRISPR-spacer integration reporter plasmids reveal distinct genuine acquisition specificities among CRISPR-Cas I-E variants of Escherichia coli. RNA Biol 10: 792-802.
16. Erdmann, S., and Garrett, R.A. (2012) Selective and hyperactive uptake of foreign DNA by adaptive immune systems of an archaeon via two distinct mechanisms. Mol Microbiol 85: 1044-1056.
17. Fineran, P.C., and Charpentier, E. (2012) Memory of viral infections by CRISPR-Cas adaptive immune systems: acquisition of new information. Virology 434: 202-209.
18. Fineran, P.C., Gerritzen, M.J., Suarez-Diez, M., Kunne, T., Boekhorst, J., van Hijum, S.A., etal. (2014) Degenerate target sites mediate rapid primed CRISPR adaptation. Proc Natl Acad Sci USA 111: E1629-E1638.
19. Garneau, J.E., Dupuis, M.E., Villion, M., Romero, D.A., Barrangou, R., Boyaval, P., etal. (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468: 67-71.
20. Goren, M., Yosef, I., Edgar, R., and Qimron, U. (2012) The bacterial CRISPR/Cas system as analog of the mammalian adaptive immune system. RNA Biol 9: 549-554.
21. Goryshin, I.Y., and Reznikoff, W.S. (1998) Tn5 in vitro transposition. J Biol Chem 273: 7367-7374.
22. Haft, D.H., Selengut, J., Mongodin, E.F., and Nelson, K.E. (2005) A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput Biol 1: e60.
23. Hale, C.R., Zhao, P., Olson, S., Duff, M.O., Graveley, B.R., Wells, L., etal. (2009) RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 139: 945-956.
24. Han, D., Lehmann, K., and Krauss, G. (2009) SSO1450 - a CAS1 protein from Sulfolobus solfataricus P2 with high affinity for RNA and DNA. FEBS Lett 583: 1928-1932.
25. Hatoum-Aslan, A., Maniv, I., and Marraffini, L.A. (2011) Mature clustered, regularly interspaced, short palindromic repeats RNA (crRNA) length is measured by a ruler mechanism anchored at the precursor processing site. Proc Natl Acad Sci USA 108: 21218-21222.
26. Hatoum-Aslan, A., Maniv, I., Samai, P., and Marraffini, L.A. (2014) Genetic Characterization of Antiplasmid Immunity through a Type III-A CRISPR-Cas System. J Bacteriol 196: 310-317.
27. Haurwitz, R.E., Jinek, M., Wiedenheft, B., Zhou, K., and Doudna, J.A. (2010) Sequence- and structure-specific RNA processing by a CRISPR endonuclease. Science 329: 1355-1358.
28. Horvath, P., Romero, D.A., Coute-Monvoisin, A.C., Richards, M., Deveau, H., Moineau, S., etal. (2008) Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol 190: 1401-1412.
29. Horvath, P., Coute-Monvoisin, A.C., Romero, D.A., Boyaval, P., Fremaux, C., and Barrangou, R. (2009) Comparative analysis of CRISPR loci in lactic acid bacteria genomes. Int J Food Microbiol 131: 62-70.
30. Ishino, Y., Shinagawa, H., Makino, K., Amemura, M., and Nakata, A. (1987) 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.
31. Jansen, R., Embden, J.D., Gaastra, W., and Schouls, L.M. (2002) Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol 43: 1565-1575.
32. Jiang, W., Bikard, D., Cox, D., Zhang, F., and Marraffini, L.A. (2013) RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31: 233-239.
33. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., and Charpentier, E. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816-821.
34. Kamerbeek, J., Schouls, L., Kolk, A., van Agterveld, M., van Soolingen, D., Kuijper, S., etal. (1997) Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol 35: 907-914.
35. Kiro, R., Goren, M.G., Yosef, I., and Qimron, U. (2013) CRISPR adaptation in Escherichia coli subtypeI-E system. Biochem Soc Trans 41: 1412-1415.
36. Kunin, V., Sorek, R., and Hugenholtz, P. (2007) Evolutionary conservation of sequence and secondary structures in CRISPR repeats. Genome Biol 8: R61.
37. Li, M., Wang, R., Zhao, D., and Xiang, H. (2013) Adaptation of the Haloarcula hispanica CRISPR-Cas system to a purified virus strictly requires a priming process. Nucleic Acids Res 42: 2483-2492.
38. Lopez-Sanchez, M.J., Sauvage, E., Da Cunha, V., Clermont, D., Ratsima Hariniaina, E., Gonzalez-Zorn, B., etal. (2012) The highly dynamic CRISPR1 system of Streptococcus agalactiae controls the diversity of its mobilome. Mol Microbiol 85: 1057-1071.
39. Makarova, K.S., Grishin, N.V., Shabalina, S.A., Wolf, Y.I., and Koonin, E.V. (2006) 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.
40. Makarova, K.S., Haft, D.H., Barrangou, R., Brouns, S.J., Charpentier, E., Horvath, P., etal. (2011) Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 9: 467-477.
41. Marraffini, L.A. (2013) CRISPR-Cas Immunity against Phages: its Effects on the Evolution and Survival of Bacterial Pathogens. PLoS Pathog 9: e1003765.
42. Marraffini, L.A., and Sontheimer, E.J. (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322: 1843-1845.
43. Marraffini, L.A., and Sontheimer, E.J. (2010) Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature 463: 568-571.
44. Merkel, G., Andrake, M.D., Ramcharan, J., and Skalka, A.M. (2009) Oligonucleotide-based assays for integrase activity. Methods 47: 243-248.
45. Mojica, F.J., Diez-Villasenor, C., Garcia-Martinez, J., and Soria, E. (2005) Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol 60: 174-182.
46. Nam, K.H., Ding, F., Haitjema, C., Huang, Q., DeLisa, M.P., and Ke, A. (2012) Double-stranded endonuclease activity in Bacillus halodurans clustered regularly interspaced short palindromic repeats (CRISPR)-associated Cas2 protein. J Biol Chem 287: 35943-35952.
47. Paez-Espino, D., Morovic, W., Sun, C.L., Thomas, B.C., Ueda, K., Stahl, B., etal. (2013) Strong bias in the bacterial CRISPR elements that confer immunity to phage. Nat Commun 4: 1430.
48. Plagens, A., Tjaden, B., Hagemann, A., Randau, L., and Hensel, R. (2012) Characterization of the CRISPR/Cas subtype I-A system of the hyperthermophilic crenarchaeon Thermoproteus tenax. J Bacteriol 194: 2491-2500.
49. Pougach, K., Semenova, E., Bogdanova, E., Datsenko, K.A., Djordjevic, M., Wanner, B.L., and Severinov, K. (2010) Transcription, processing and function of CRISPR cassettes in Escherichia coli. Mol Microbiol 77: 1367-1379.
50. Pourcel, C., Salvignol, G., and Vergnaud, G. (2005) 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.
51. Pride, D.T., Sun, C.L., Salzman, J., Rao, N., Loomer, P., Armitage, G.C., etal. (2011) Analysis of streptococcal CRISPRs from human saliva reveals substantial sequence diversity within and between subjects over time. Genome Res 21: 126-136.
52. Pride, D.T., Salzman, J., and Relman, D.A. (2012) Comparisons of clustered regularly interspaced short palindromic repeats and viromes in human saliva reveal bacterial adaptations to salivary viruses. Environ Microbiol 14: 2564-2576.
53. Samai, P., Smith, P., and Shuman, S. (2010) Structure of a CRISPR-associated protein Cas2 from Desulfovibrio vulgaris. Acta Crystallogr Sect F Struct Biol Cryst Commun 66: 1552-1556.
54. Sapranauskas, R., Gasiunas, G., Fremaux, C., Barrangou, R., Horvath, P., and Siksnys, V. (2011) The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res 39: 9275-9282.
55. Savitskaya, E., Semenova, E., Dedkov, V., Metlitskaya, A., and Severinov, K. (2013) High-throughput analysis of type I-E CRISPR/Cas spacer acquisition in E. coli. RNA Biol 10: 716-725.
56. Semenova, E., Jore, M.M., Datsenko, K.A., Semenova, A., Westra, E.R., Wanner, B., etal. (2011) Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc Natl Acad Sci USA 108: 10098-10103.
57. Shah, S.A., Hansen, N.R., and Garrett, R.A. (2009) Distribution of CRISPR spacer matches in viruses and plasmids of crenarchaeal acidothermophiles and implications for their inhibitory mechanism. Biochem Soc Trans 37: 23-28.
58. Shmakov, S., Savitskaya, E., Semenova, E., Logacheva, M.D., Datsenko, K.A., and Severinov, K. (2014) Pervasive generation of oppositely oriented spacers during CRISPR adaptation. Nucleic Acids Res 42: 5907-5916. doi: 10.1093/nar/gku226.
59. Sorek, R., Kunin, V., and Hugenholtz, P. (2008) CRISPR-a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 6: 181-186.
60. Swarts, D.C., Mosterd, C., van Passel, M.W., and Brouns, S.J. (2012) CRISPR interference directs strand specific spacer acquisition. PLoS ONE 7: e35888.
61. Thomas, C.M., and Nielsen, K.M. (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3: 711-721.
62. Tyson, G.W., and Banfield, J.F. (2008) Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microbiol 10: 200-2007.
63. Westra, E.R., van Erp, P.B., Kunne, T., Wong, S.P., Staals, R.H., Seegers, C.L., etal. (2012) CRISPR immunity relies on the consecutive binding and degradation of negatively supercoiled invader DNA by Cascade and Cas3. Mol Cell 46: 595-605.
64. Westra, E.R., Semenova, E., Datsenko, K.A., Jackson, R.N., Wiedenheft, B., Severinov, K., and Brouns, S.J. (2013) Type I-E CRISPR-cas systems discriminate target from non-target DNA through base pairing-independent PAM recognition. PLoS Genet 9: e1003742.
65. Wiedenheft, B., Zhou, K., Jinek, M., Coyle, S.M., Ma, W., and Doudna, J.A. (2009) Structural basis for DNase activity of a conserved protein implicated in CRISPR-mediated genome defense. Structure 17: 904-912.
66. Yosef, I., Goren, M.G., and Qimron, U. (2012) Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res 40: 5569-5576.
67. Yosef, I., Shitrit, D., Goren, M.G., Burstein, D., Pupko, T., and Qimron, U. (2013) DNA motifs determining the efficiency of adaptation into the Escherichia coli CRISPR array. Proc Natl Acad Sci USA 110: 14396-14401.
68. Zhang, Y., Heidrich, N., Ampattu, B.J., Gunderson, C.W., Seifert, H.S., Schoen, C., etal. (2013) Processing-independent CRISPR RNAs limit natural transformation in Neisseria meningitidis. Mol Cell 50: 488-503.