CRISPR-Cas Systems Optimize Their Immune Response by Specifying the Site of Spacer Integration

Molecular Cell

Volumn 64, Issue 3, 2016, Pages 616-623

  McGinn, Jon ^a   Marraffini, Luciano A ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SPACER DNA; 5' UNTRANSLATED REGION; BACTERIAL PROTEIN; CAS9 ENDONUCLEASE STREPTOCOCCUS PYOGENES; CRISPR ASSOCIATED PROTEIN; ENDONUCLEASE;

ARTICLE; BACTERIAL IMMUNITY; CONSERVED SEQUENCE; CONTROLLED STUDY; CRISPR CAS SYSTEM; DNA INTEGRATION; GENE MUTATION; IMMUNE RESPONSE; NONHUMAN; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PYOGENES; 5' UNTRANSLATED REGION; BACTERIAL CHROMOSOME; BACTERIOPHAGE; CHEMISTRY; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; GENE EXPRESSION REGULATION; GENE LOCUS; GENETICS; IMMUNOLOGY; METABOLISM; NUCLEOTIDE SEQUENCE; VIROLOGY;

5' UNTRANSLATED REGIONS; BACTERIAL PROTEINS; BACTERIOPHAGES; BASE SEQUENCE; CHROMOSOMES, BACTERIAL; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; ENDONUCLEASES; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC LOCI; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PYOGENES;

EID: 84994798354     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.08.038     Document Type: Article

References (38)

1. Andersson, A.F., Banfield, J.F., Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320 (2008), 1047–1050.
2. Arslan, Z., Hermanns, V., Wurm, R., Wagner, R., Pul, Ü., Detection and characterization of spacer integration intermediates in type I-E CRISPR-Cas system. Nucleic Acids Res. 42 (2014), 7884–7893.
3. 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 315 (2007), 1709–1712.
4. 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 321 (2008), 960–964.
5. 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. 22 (2008), 3489–3496.
6. Chylinski, K., Le Rhun, A., Charpentier, E., The tracrRNA and Cas9 families of type II CRISPR-Cas immunity systems. RNA Biol. 10 (2013), 726–737.
7. Datsenko, K.A., Pougach, K., Tikhonov, A., Wanner, B.L., Severinov, K., Semenova, E., Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system. Nat. Commun., 3, 2012, 945.
8. Deltcheva, E., Chylinski, K., Sharma, C.M., Gonzales, K., Chao, Y., Pirzada, Z.A., Eckert, M.R., Vogel, J., Charpentier, E., CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471 (2011), 602–607.
9. Deveau, H., Barrangou, R., Garneau, J.E., Labonté, J., Fremaux, C., Boyaval, P., Romero, D.A., Horvath, P., Moineau, S., Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol. 190 (2008), 1390–1400.
10. Elmore, J.R., Yokooji, Y., Sato, T., Olson, S., Glover, C.V. 3rd, Graveley, B.R., Atomi, H., Terns, R.M., Terns, M.P., Programmable plasmid interference by the CRISPR-Cas system in Thermococcus kodakarensis. RNA Biol. 10 (2013), 828–840.
11. Garneau, J.E., Dupuis, M.E., Villion, M., Romero, D.A., Barrangou, R., Boyaval, P., Fremaux, C., Horvath, P., Magadán, A.H., Moineau, S., The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468 (2010), 67–71.
12. Gasiunas, G., Barrangou, R., Horvath, P., Siksnys, V., Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc. Natl. Acad. Sci. USA 109 (2012), E2579–E2586.
13. Heler, R., Samai, P., Modell, J.W., Weiner, C., Goldberg, G.W., Bikard, D., Marraffini, L.A., Cas9 specifies functional viral targets during CRISPR-Cas adaptation. Nature 519 (2015), 199–202.
14. Horinouchi, S., Weisblum, B., Nucleotide sequence and functional map of pC194, a plasmid that specifies inducible chloramphenicol resistance. J. Bacteriol. 150 (1982), 815–825.
15. Jansen, R., Embden, J.D., Gaastra, W., Schouls, L.M., Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43 (2002), 1565–1575.
16. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., Charpentier, E., A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337 (2012), 816–821.
17. Jore, M.M., Lundgren, M., van Duijn, E., Bultema, J.B., Westra, E.R., Waghmare, S.P., Wiedenheft, B., Pul, U., Wurm, R., Wagner, R., et al. Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat. Struct. Mol. Biol. 18 (2011), 529–536.
18. Kreiswirth, B.N., Löfdahl, S., Betley, M.J., O'Reilly, M., Schlievert, P.M., Bergdoll, M.S., Novick, R.P., The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305 (1983), 709–712.
19. Makarova, K.S., Wolf, Y.I., Alkhnbashi, O.S., Costa, F., Shah, S.A., Saunders, S.J., Barrangou, R., Brouns, S.J., Charpentier, E., Haft, D.H., et al. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13 (2015), 722–736.
20. Marraffini, L.A., Sontheimer, E.J., CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322 (2008), 1843–1845.
21. Murphy, K., Travers, P., Walport, M., Janeway, C., Janeway's immunobiology. 2012, Garland Science, New York.
22. Nickel, L., Weidenbach, K., Jäger, D., Backofen, R., Lange, S.J., Heidrich, N., Schmitz, R.A., Two CRISPR-Cas systems in Methanosarcina mazei strain Gö1 display common processing features despite belonging to different types I and III. RNA Biol. 10 (2013), 779–791.
23. Nuñez, J.K., Kranzusch, P.J., Noeske, J., Wright, A.V., Davies, C.W., Doudna, J.A., Cas1-Cas2 complex formation mediates spacer acquisition during CRISPR-Cas adaptive immunity. Nat. Struct. Mol. Biol. 21 (2014), 528–534.
24. Nuñez, J.K., Lee, A.S., Engelman, A., Doudna, J.A., Integrase-mediated spacer acquisition during CRISPR-Cas adaptive immunity. Nature 519 (2015), 193–198.
25. Nuñez, J.K., Bai, L., Harrington, L.B., Hinder, T.L., Doudna, J.A., CRISPR Immunological Memory Requires a Host Factor for Specificity. Mol. Cell 62 (2016), 824–833.
26. Perez-Casal, J., Caparon, M.G., Scott, J.R., Mry, a trans-acting positive regulator of the M protein gene of Streptococcus pyogenes with similarity to the receptor proteins of two-component regulatory systems. J. Bacteriol. 173 (1991), 2617–2624.
27. Randau, L., RNA processing in the minimal organism Nanoarchaeum equitans. Genome Biol., 13, 2012, R63.
28. Richter, H., Zoephel, J., Schermuly, J., Maticzka, D., Backofen, R., Randau, L., Characterization of CRISPR RNA processing in Clostridium thermocellum and Methanococcus maripaludis. Nucleic Acids Res. 40 (2012), 9887–9896.
29. Rollie, C., Schneider, S., Brinkmann, A.S., Bolt, E.L., White, M.F., Intrinsic sequence specificity of the Cas1 integrase directs new spacer acquisition. eLife, 4, 2015, 4.
30. Samai, P., Pyenson, N., Jiang, W., Goldberg, G.W., Hatoum-Aslan, A., Marraffini, L.A., Co-transcriptional DNA and RNA Cleavage during Type III CRISPR-Cas Immunity. Cell 161 (2015), 1164–1174.
31. Shmakov, S., Abudayyeh, O.O., Makarova, K.S., Wolf, Y.I., Gootenberg, J.S., Semenova, E., Minakhin, L., Joung, J., Konermann, S., Severinov, K., et al. Discovery and Functional Characterization of Diverse Class 2 CRISPR-Cas Systems. Mol. Cell 60 (2015), 385–397.
32. Sternberg, S.H., Redding, S., Jinek, M., Greene, E.C., Doudna, J.A., DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507 (2014), 62–67.
33. Sun, C.L., Barrangou, R., Thomas, B.C., Horvath, P., Fremaux, C., Banfield, J.F., Phage mutations in response to CRISPR diversification in a bacterial population. Environ. Microbiol. 15 (2013), 463–470.
34. Wei, Y., Terns, M.P., CRISPR Outsourcing: Commissioning IHF for Site-Specific Integration of Foreign DNA at the CRISPR Array. Mol. Cell 62 (2016), 803–804.
35. Wei, Y., Chesne, M.T., Terns, R.M., Terns, M.P., Sequences spanning the leader-repeat junction mediate CRISPR adaptation to phage in Streptococcus thermophilus. Nucleic Acids Res. 43 (2015), 1749–1758.
36. Weinberger, A.D., Sun, C.L., Pluciński, M.M., Denef, V.J., Thomas, B.C., Horvath, P., Barrangou, R., Gilmore, M.S., Getz, W.M., Banfield, J.F., Persisting viral sequences shape microbial CRISPR-based immunity. PLoS Comput. Biol., 8, 2012, e1002475.
37. 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 17 (2009), 904–912.
38. Yosef, I., Goren, M.G., Qimron, U., Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res. 40 (2012), 5569–5576.