DNA targeting by the type I-G and type I-A CRISPR-Cas systems of Pyrococcus furiosus

Nucleic Acids Research

Volumn 43, Issue 21, 2015, Pages 10353-10363

  Elmore, Joshua ^a   Deighan, Trace ^a   Westpheling, Jan ^a   Terns, Rebecca M ^a   Terns, Michael P ^a,b  

^a University of Georgia   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; ARCHAEAL RNA; CRISPR ASSOCIATED PROTEIN; DEOXYRIBONUCLEASE; DNA;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; COMPLEX FORMATION; CONTROLLED STUDY; CRISPR CAS SYSTEM; DNA FLANKING REGION; GENE IDENTIFICATION; GENE LOCUS; GENE SILENCING; GENE TARGETING; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PYROCOCCUS FURIOSUS; GENETICS; METABOLISM; PLASMID;

CRISPR-ASSOCIATED PROTEINS; CRISPR-CAS SYSTEMS; DEOXYRIBONUCLEASES; DNA; PLASMIDS; PYROCOCCUS FURIOSUS; RNA, ARCHAEAL;

EID: 84956770932     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1140     Document Type: Article

References (79)

1. Terns, M.P. and Terns, R.M. (2011) CRISPR-based adaptive immune systems. Curr. Opin. Microbiol., 14, 321-327.
2. van der Oost, J., Westra, E.R., Jackson, R.N. and Wiedenheft, B. (2014) Unravelling the structural and mechanistic basis of CRISPR-Cas systems. Nat. Rev. Microbiol., 12, 479-492.
3. Tsui, T.K. and Li, H. (2015) Structure Principles of CRISPR-Cas Surveillance and Effector Complexes. Annu. Rev. Biophys., 44, 229-255.
4. Jackson, R.N. and Wiedenheft, B. (2015) A conserved structural chassis for mounting versatile CRISPR RNA-guided immune responses. Mol. Cell, 58, 722-728.
5. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D.A. and Horvath, P. (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science, 315, 1709-1712.
6. Elmore, J.R., Yokooji, Y., Sato, T., Olson, S., Glover, C.V. 3rd, Graveley, B.R., Atomi, H., Terns, R.M. and Terns, M.P. (2013) Programmable plasmid interference by the CRISPR-Cas system in Thermococcus kodakarensis. RNA Biol., 10, 828-840.
7. Garneau, J.E., Dupuis, M.E., Villion, M., Romero, D.A., Barrangou, R., Boyaval, P., Fremaux, C., Horvath, P., Magadan, A.H. and Moineau, S. (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature, 468, 67-71.
8. Hale, C.R., Majumdar, S., Elmore, J., Pfister, N., Compton, M., Olson, S., Resch, A.M., Glover, C.V. 3rd, Graveley, B.R., Terns, R.M. et al. (2012) Essential features and rational design of CRISPR RNAs that function with the Cas RAMP module complex to cleave RNAs. Mol. Cell, 45, 292-302.
9. 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. (2011) Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat. Struct. Mol. Biol., 18, 529-536.
10. Lintner, N.G., Kerou, M., Brumfield, S.K., Graham, S., Liu, H., Naismith, J.H., Sdano, M., Peng, N., She, Q., Copie, V. et al. (2011) Structural and functional characterization of an archaeal clustered regularly interspaced short palindromic repeat (CRISPR)-associated complex for antiviral defense (CASCADE). J. Biol. Chem., 286, 21643-21656.
11. Maier, L.K., Lange, S.J., Stoll, B., Haas, K.A., Fischer, S., Fischer, E., Duchardt-Ferner, E., Wohnert, J., Backofen, R. and Marchfelder, A. (2013) Essential requirements for the detection and degradation of invaders by the Haloferax volcanii CRISPR/Cas system I-B. RNA Biol., 10, 865-874.
12. Marraffini, L.A. and Sontheimer, E.J. (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science, 322, 1843-1845.
13. Mulepati, S. and Bailey, S. (2013) In vitro reconstitution of an Escherichia coli RNA-guided immune system reveals unidirectional, ATP-dependent degradation of DNA target. J. Biol. Chem., 288, 22184-22192.
14. Peng, W., Li, H., Hallstrom, S., Peng, N., Liang, Y.X. and She, Q. (2013) Genetic determinants of PAM-dependent DNA targeting and pre-crRNA processing in Sulfolobus islandicus. RNA Biol. 10, 738-748.
15. Sinkunas, T., Gasiunas, G., Waghmare, S.P., Dickman, M.J., Barrangou, R., Horvath, P. and Siksnys, V. (2013) In vitro reconstitution of Cascade-mediated CRISPR immunity in Streptococcus thermophilus. EMBO J., 32, 385-394.
16. Westra, E.R., van Erp, P.B., Kunne, T., Wong, S.P., Staals, R.H., Seegers, C.L., Bollen, S., Jore, M.M., Semenova, E., Severinov, K. et al. (2012) CRISPR immunity relies on the consecutive binding and degradation of negatively supercoiled invader DNA by Cascade and Cas3. Mol. Cell, 46, 595-605.
17. Wiedenheft, B., Lander, G.C., Zhou, K., Jore, M.M., Brouns, S.J., van der Oost, J., Doudna, J.A. and Nogales, E. (2011) Structures of the RNA-guided surveillance complex from a bacterial immune system. Nature, 477, 486-489.
18. Makarova, K.S., Haft, D.H., Barrangou, R., Brouns, S.J., Charpentier, E., Horvath, P., Moineau, S., Mojica, F.J., Wolf, Y.I., Yakunin, A.F. et al. (2011) Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol., 9, 467-477.
19. Vestergaard, G., Garrett, R.A. and Shah, S.A. (2014) CRISPR adaptive immune systems of Archaea. RNA Biol., 11, 156-167.
20. Plagens, A., Tripp, V., Daume, M., Sharma, K., Klingl, A., Hrle, A., Conti, E., Urlaub, H. and Randau, L. (2014) In vitro assembly and activity of an archaeal CRISPR-Cas type I-A Cascade interference complex. Nucleic Acids Res., 42, 5125-5138.
21. 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.
22. Karvelis, T., Gasiunas, G. and Siksnys, V. (2013) Programmable DNA cleavage in vitro by Cas9. Biochem. Soc. Trans., 41, 1401-1406.
23. Hale, C.R., Zhao, P., Olson, S., Duff, M.O., Graveley, B.R., Wells, L., Terns, R.M. and Terns, M.P. (2009) RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell, 139, 945-956.
24. Zhang, J., Rouillon, C., Kerou, M., Reeks, J., Brugger, K., Graham, S., Reimann, J., Cannone, G., Liu, H., Albers, S.V. et al. (2012) Structure and mechanism of the CMR complex for CRISPR-mediated antiviral immunity. Mol. cell, 45, 303-313.
25. Staals, R.H., Agari, Y., Maki-Yonekura, S., Zhu, Y., Taylor, D.W., van Duijn, E., Barendregt, A., Vlot, M., Koehorst, J.J., Sakamoto, K. et al. (2013) Structure and activity of the RNA-targeting Type III-B CRISPR-Cas complex of Thermus thermophilus. Mol. Cell, 52, 135-145.
26. Staals, R.H., Zhu, Y., Taylor, D.W., Kornfeld, J.E., Sharma, K., Barendregt, A., Koehorst, J.J., Vlot, M., Neupane, N., Varossieau, K. et al. (2014) RNA targeting by the type III-A CRISPR-Cas Csm complex of Thermus thermophilus. Mol. Cell, 56, 518-530.
27. Tamulaitis, G., Kazlauskiene, M., Manakova, E., Venclovas, C., Nwokeoji, A.O., Dickman, M.J., Horvath, P. and Siksnys, V. (2014) Programmable RNA shredding by the type III-A CRISPR-Cas system of Streptococcus thermophilus. Mol. Cell, 56, 506-517.
28. Samai, P., Pyenson, N., Jiang, W., Goldberg, G.W., Hatoum-Aslan, A. and Marraffini, L.A. (2015) Co-transcriptional DNA and RNA Cleavage during Type III CRISPR-Cas Immunity. Cell, 161, 1164-1174.
29. Hochstrasser, M.L., Taylor, D.W., Bhat, P., Guegler, C.K., Sternberg, S.H., Nogales, E. and Doudna, J.A. (2014) CasA mediates Cas3-catalyzed target degradation during CRISPR RNA-guided interference. Proc. Natl. Acad. Sci. U.S.A., 111, 6618-6623.
30. Deveau, H., Barrangou, R., Garneau, J.E., Labonte, J., Fremaux, C., Boyaval, P., Romero, D.A., Horvath, P. and Moineau, S. (2008) Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol., 190, 1390-1400.
31. Mojica, F.J., Diez-Villasenor, C., Garcia-Martinez, J. and Almendros, C. (2009) Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology, 155, 733-740.
32. Shah, S.A., Erdmann, S., Mojica, F.J. and Garrett, R.A. (2013) Protospacer recognition motifs: mixed identities and functional diversity. RNA Biol., 10, 891-899.
33. 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.
34. 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.
35. Fischer, S., Maier, L.K., Stoll, B., Brendel, J., Fischer, E., Pfeiffer, F., Dyall-Smith, M. and Marchfelder, A. (2012) An archaeal immune system can detect multiple protospacer adjacent motifs (PAMs) to target invader DNA. J. Biol. Chem., 287, 33351-33363.
36. Gudbergsdottir, S., Deng, L., Chen, Z., Jensen, J.V., Jensen, L.R., She, Q. and Garrett, R.A. (2011) Dynamic properties of the Sulfolobus CRISPR/Cas and CRISPR/Cmr systems when challenged with vector-borne viral and plasmid genes and protospacers. Mol. Microbiol., 79, 35-49.
37. Manica, A., Zebec, Z., Teichmann, D. and Schleper, C. (2011) In vivo activity of CRISPR-mediated virus defence in a hyperthermophilic archaeon. Mol. Microbiol., 80, 481-491.
38. 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.
39. 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.
40. Westra, E.R., Swarts, D.C., Staals, R.H., Jore, M.M., Brouns, S.J. and van der Oost, J. (2012) The CRISPRs, they are a-changin': how prokaryotes generate adaptive immunity. Annu. Rev. Genet., 46, 311-339.
41. Carte, J., Christopher, R.T., Smith, J.T., Olson, S., Barrangou, R., Moineau, S., Glover, C.V. 3rd, Graveley, B.R., Terns, R.M. and Terns, M.P. (2014) The three major types of CRISPR-Cas systems function independently in CRISPR RNA biogenesis in Streptococcus thermophilus. Mol. Microbiol., 93, 98-112.
42. Deltcheva, E., Chylinski, K., Sharma, C.M., Gonzales, K., Chao, Y., Pirzada, Z.A., Eckert, M.R., Vogel, J. and Charpentier, E. (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature, 471, 602-607.
43. Wei, Y., Terns, R.M. and Terns, M.P. (2015) Cas9 function and host genome sampling in Type II-A CRISPR-Cas adaptation. Genes Dev., 29, 356-361.
44. Terns, R.M. and Terns, M.P. (2013) The RNA- and DNA-targeting CRISPR-Cas immune systems of Pyrococcus furiosus. Biochem. Soc. Trans., 41, 1416-1421.
45. Majumdar, S., Zhao, P., Pfister, N.T., Compton, M., Olson, S., Glover, C.V. 3rd, Wells, L., Graveley, B.R., Terns, R.M. and Terns, M.P. (2015) Three CRISPR-Cas immune effector complexes coexist in Pyrococcus furiosus. RNA.
46. Carte, J., Wang, R., Li, H., Terns, R.M. and Terns, M.P. (2008) Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev., 22, 3489-3496.
47. Carte, J., Pfister, N.T., Compton, M.M., Terns, R.M. and Terns, M.P. (2010) Binding and cleavage of CRISPR RNA by Cas6. RNA, 16, 2181-2188.
48. Hale, C., Kleppe, K., Terns, R.M. and Terns, M.P. (2008) Prokaryotic silencing (psi)RNAs in Pyrococcus furiosus. RNA, 14, 2572-2579.
49. Ramia, N.F., Spilman, M., Tang, L., Shao, Y., Elmore, J., Hale, C., Cocozaki, A., Bhattacharya, N., Terns, R.M., Terns, M.P. et al. (2014) Essential structural and functional roles of the Cmr4 subunit in RNA cleavage by the Cmr CRISPR-Cas complex. Cell Rep., 9, 1610-1617.
50. Spilman, M., Cocozaki, A., Hale, C., Shao, Y., Ramia, N., Terns, R., Terns, M., Li, H. and Stagg, S. (2013) Structure of an RNA silencing complex of the CRISPR-Cas immune system. Mol. Cell, 52, 146-152.
51. Hale, C.R., Cocozaki, A., Li, H., Terns, R.M. and Terns, M.P. (2014) Target RNA capture and cleavage by the Cmr type III-B CRISPR-Cas effector complex. Genes Dev., 28, 2432-2443.
52. Lipscomb, G.L., Stirrett, K., Schut, G.J., Yang, F., Jenney, F.E. Jr, Scott, R.A., Adams, M.W. and Westpheling, J. (2011) Natural competence in the hyperthermophilic archaeon Pyrococcus furiosus facilitates genetic manipulation: construction of markerless deletions of genes encoding the two cytoplasmic hydrogenases. Appl. Environ. Microbiol., 77, 2232-2238.
53. Farkas, J., Chung, D., DeBarry, M., Adams, M.W. and Westpheling, J. (2011) Defining components of the chromosomal origin of replication of the hyperthermophilic archaeon Pyrococcus furiosus needed for construction of a stable replicating shuttle vector. Appl. Environ. Microbiol., 77, 6343-6349.
54. Farkas, J., Stirrett, K., Lipscomb, G.L., Nixon, W., Scott, R.A., Adams, M.W. and Westpheling, J. (2012) Recombinogenic properties of Pyrococcus furiosus strain COM1 enable rapid selection of targeted mutants. Appl. Environ. Microbiol., 78, 4669-4676.
55. Han, D. and Krauss, G. (2009) Characterization of the endonuclease SSO2001 from Sulfolobus solfataricus P2. FEBS Lett., 583, 771-776.
56. Beloglazova, N., Petit, P., Flick, R., Brown, G., Savchenko, A. and Yakunin, A.F. (2011) Structure and activity of the Cas3 HD nuclease MJ0384, an effector enzyme of the CRISPR interference. EMBO J., 30, 4616-4627.
57. Howard, J.A., Delmas, S., Ivancic-Bace, I. and Bolt, E.L. (2011) Helicase dissociation and annealing of RNA-DNA hybrids by Escherichia coli Cas3 protein. Biochem. J., 439, 85-95.
58. Mulepati, S. and Bailey, S. (2011) Structural and biochemical analysis of nuclease domain of clustered regularly interspaced short palindromic repeat (CRISPR)-associated protein 3 (Cas3). J. Biol. Chem., 286, 31896-31903.
59. Sinkunas, T., Gasiunas, G., Fremaux, C., Barrangou, R., Horvath, P. and Siksnys, V. (2011) Cas3 is a single-stranded DNA nuclease and ATP-dependent helicase in the CRISPR/Cas immune system. EMBO J., 30, 1335-1342.
60. Huo, Y., Nam, K.H., Ding, F., Lee, H., Wu, L., Xiao, Y., Farchione, M.D. Jr, Zhou, S., Rajashankar, K., Kurinov, I. et al. (2014) Structures of CRISPR Cas3 offer mechanistic insights into Cascade-activated DNA unwinding and degradation. Nat. Struct. Mol. Biol., 21, 771-777.
61. 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.
62. Jackson, R.N., Lavin, M., Carter, J. and Wiedenheft, B. (2014) Fitting CRISPR-associated Cas3 into the Helicase Family Tree. Curr. Opin. Struct. Biol., 24, 106-114.
63. Menon, A.L., Poole, F.L. 2nd, Cvetkovic, A., Trauger, S.A., Kalisiak, E., Scott, J.W., Shanmukh, S., Praissman, J., Jenney, F.E. Jr, Wikoff, W.R. et al. (2009) Novel multiprotein complexes identified in the hyperthermophilic archaeon Pyrococcus furiosus by non-denaturing fractionation of the native proteome. Mol. Cell. Proteomics : MCP, 8, 735-751.
64. 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.
65. 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. and van der Oost, J. (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science, 321, 960-964.
66. 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.
67. 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.
68. 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. U.S.A., 108, 21218-21222.
69. Wiedenheft, B., van Duijn, E., Bultema, J.B., Waghmare, S.P., Zhou, K., Barendregt, A., Westphal, W., Heck, A.J., Boekema, E.J., Dickman, M.J. et al. (2011) RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Proc. Natl. Acad. Sci. U.S.A., 108, 10092-10097.
70. Jackson, R.N., Golden, S.M., van Erp, P.B., Carter, J., Westra, E.R., Brouns, S.J., van der Oost, J., Terwilliger, T.C., Read, R.J. and Wiedenheft, B. (2014) Structural biology. Crystal structure of the CRISPR RNA-guided surveillance complex from Escherichia coli. Science, 345, 1473-1479.
71. Mulepati, S., Heroux, A. and Bailey, S. (2014) Structural biology. Crystal structure of a CRISPR RNA-guided surveillance complex bound to a ssDNA target. Science, 345, 1479-1484.
72. Zhao, H., Sheng, G., Wang, J., Wang, M., Bunkoczi, G., Gong, W., Wei, Z. and Wang, Y. (2014) Crystal structure of the RNA-guided immune surveillance Cascade complex in Escherichia coli. Nature.
73. Kunin, V., Sorek, R. and Hugenholtz, P. (2007) Evolutionary conservation of sequence and secondary structures in CRISPR repeats. Genome Biol., 8, R61.
74. 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.
75. Semenova, E., Jore, M.M., Datsenko, K.A., Semenova, A., Westra, E.R., Wanner, B., van der Oost, J., Brouns, S.J. and Severinov, K. (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.
76. Williams, E., Lowe, T.M., Savas, J. and DiRuggiero, J. (2007) Microarray analysis of the hyperthermophilic archaeon Pyrococcus furiosus exposed to gamma irradiation. Extremophiles, 11, 19-29.
77. Strand, K.R., Sun, C., Li, T., Jenney, F.E. Jr, Schut, G.J. and Adams, M.W. (2010) Oxidative stress protection and the repair response to hydrogen peroxide in the hyperthermophilic archaeon Pyrococcus furiosus and in related species. Arch. Microbiol., 192, 447-459.
78. Pawluk, A., Bondy-Denomy, J., Cheung, V.H., Maxwell, K.L. and Davidson, A.R. (2014) A new group of phage anti-CRISPR genes inhibits the type I-E CRISPR-Cas system of Pseudomonas aeruginosa. mBio, 5, e00896.
79. Bondy-Denomy, J., Pawluk, A., Maxwell, K.L. and Davidson, A.R. (2013) Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature, 493, 429-432.