CRISPR-mediated adaptive immune systems in bacteria and archaea
Open accessAbstract
Effective clearance of an infection requires that the immune system rapidly detects and neutralizes invading parasites while strictly avoiding self-antigens that would result in autoimmunity. The cellular machinery and complex signaling pathways that coordinate an effective immune response have generally been considered properties of the eukaryotic immune system. However, a surprisingly sophisticated adaptive immune system that relies on small RNAs for sequence-specific targeting of foreign nucleic acids was recently discovered in bacteria and archaea. Molecular vaccination in prokaryotes is achieved by integrating short fragments of foreign nucleic acids into a repetitive locus in the host chromosome known as a CRISPR (clustered regularly interspaced short palindromic repeat). Here we review the mechanisms of CRISPR-mediated immunity and discuss the ecological and evolutionary implications of these adaptive defense systems.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A Programmable Dual-RNA–Guided DNA Endonuclease in Adaptive Bacterial Immunity
Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., & Charpentier, E. (2012) · Science · doi:10.1126/science.1225829 · Cited by 17,116 · see citing works
A human gut microbial gene catalogue established by metagenomic sequencing
MetaHIT Consortium, Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., et al. (2010) · Nature · doi:10.1038/nature08821 · Cited by 11,624 · see citing works
CRISPR Provides Acquired Resistance Against Viruses in Prokaryotes
Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D. A., & Horvath, P. (2007) · Science · doi:10.1126/science.1138140 · Cited by 6,304 · see citing works
Small CRISPR RNAs Guide Antiviral Defense in Prokaryotes
Brouns, S. J. J., Jore, M. M., Lundgren, M., Westra, E. R., Slijkhuis, R. J. H., Snijders, A. P., Dickman, M. J., Makarova, K. S., Koonin, E. V., & John van der, O. O. S. T. (2008) · Science · doi:10.1126/science.1159689 · Cited by 2,593 · see citing works
CRISPR RNA Maturation by Trans-Encoded Small RNA and Host Factor RNase III
Deltcheva, E., Chylinski, K., Sharma, C. M., Gonzales, K., Chao, Y., Pirzada, Z. A., Eckert, M. R., Vogel, J., & Charpentier, E. (2011) · Nature · doi:10.1038/nature09886 · Cited by 2,563 · see citing works
Evolution and classification of the CRISPR–Cas systems
Makarova, K. S., Haft, D. H., Barrangou, R., Brouns, S. J. J., Charpentier, E., Horvath, P., Moineau, S., Mojica, F. J. M., Wolf, Y. I., Yakunin, A. F., et al. (2011) · Nature Reviews Microbiology · doi:10.1038/nrmicro2577 · Cited by 2,512 · see citing works
CRISPR/Cas, the Immune System of Bacteria and Archaea
Horvath, P., & Barrangou, R. (2010) · Science · doi:10.1126/science.1179555 · Cited by 2,471 · see citing works
Ishino, Y., Shinagawa, H., Makino, K., Amemura, M., & Nakata, A. (1987) · Journal of Bacteriology · doi:10.1128/jb.169.12.5429-5433.1987 · Cited by 2,421 · see citing works
The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA
Garneau, J. E., Dupuis, M.-È., Villion, M., Romero, D. A., Barrangou, R., Boyaval, P., Fremaux, C., Horvath, P., Magadán, A. H., & Moineau, S. (2010) · Nature · doi:10.1038/nature09523 · Cited by 2,336 · see citing works
Intervening Sequences of Regularly Spaced Prokaryotic Repeats Derive from Foreign Genetic Elements
Mojica, F. J. M., D�ez-Villase�or, C., Garc�a-Mart�nez, J., & Soria, E. (2005) · Journal of Molecular Evolution · doi:10.1007/s00239-004-0046-3 · Cited by 2,219 · see citing works
Suttle, C. A. (2005) · Nature · doi:10.1038/nature04160 · Cited by 2,186 · see citing works
Identification of genes that are associated with DNA repeats in prokaryotes
Jansen, R., van Embden, J. D. A., Gaastra, W., & Schouls, L. M. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.02839.x · Cited by 2,035 · see citing works
CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats
Grissa, I., Vergnaud, G., & Pourcel, C. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm360 · Cited by 1,877 · see citing works
RNA-guided genetic silencing systems in bacteria and archaea
Wiedenheft, B., Sternberg, S. H., & Doudna, J. A. (2012) · Nature · doi:10.1038/nature10886 · Cited by 1,851 · see citing works
Self-citationEcology of prokaryotic viruses
Weinbauer, M. G. (2003) · FEMS Microbiology Reviews · doi:10.1016/j.femsre.2003.08.001 · Cited by 1,776 · see citing works
CRISPR Interference Limits Horizontal Gene Transfer in Staphylococci by Targeting DNA
Marraffini, L. A., & Sontheimer, E. J. (2008) · Science · doi:10.1126/science.1165771 · Cited by 1,752 · see citing works
Bolotin, A., Quinquis, B., Sorokin, A., & Ehrlich, S. D. (2005) · Microbiology · doi:10.1099/mic.0.28048-0 · Cited by 1,733 · see citing works
High abundance of viruses found in aquatic environments
Bergh, Ø., Børsheim, K. Y., Bratbak, G., & Heldal, M. (1989) · Nature · doi:10.1038/340467a0 · Cited by 1,650 · see citing works
Short motif sequences determine the targets of the prokaryotic CRISPR defence system
Mojica, F. J. M., Díez‐Villaseñor, C., García‐Martínez, J., & Almendros, C. (2009) · Microbiology · doi:10.1099/mic.0.023960-0 · Cited by 1,500 · see citing works
Pourcel, C., Salvignol, G., & Vergnaud, G. (2005) · Microbiology · doi:10.1099/mic.0.27437-0 · Cited by 1,347 · see citing works
Makarova, K. S., Grishin, N. V., Shabalina, S. A., Wolf, Y. I., & Koonin, E. V. (2006) · Biology Direct · doi:10.1186/1745-6150-1-7 · Cited by 1,199 · see citing works
Phage Response to CRISPR-Encoded Resistance in Streptococcus thermophilus
Deveau, H., Barrangou, R., Garneau, J. E., Labonté, J., Fremaux, C., Boyaval, P., Romero, D. A., Horvath, P., & Moineau, S. (2007) · Journal of Bacteriology · doi:10.1128/jb.01412-07 · Cited by 1,196 · see citing works
Potrykus, K., & Cashel, M. (2008) · Annual Review of Microbiology · doi:10.1146/annurev.micro.62.081307.162903 · Cited by 1,170 · see citing works
Maris, C., Dominguez, C., & Allain, F. H. ‐. (2005) · FEBS Journal · doi:10.1111/j.1742-4658.2005.04653.x · Cited by 1,135 · see citing works
RNA-Guided RNA Cleavage by a CRISPR RNA-Cas Protein Complex
Hale, C. R., Zhao, P., Olson, S., Duff, M. O., Graveley, B. R., Wells, L., Terns, R. M., & Terns, M. P. (2009) · Cell · doi:10.1016/j.cell.2009.07.040 · Cited by 1,031 · see citing works
CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea
Marraffini, L. A., & Sontheimer, E. J. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2749 · Cited by 1,011 · see citing works
Haft, D. H., Selengut, J., Mongodin, E. F., & Nelson, K. E. (2005) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0010060 · Cited by 981 · see citing works
The human gut virome: inter-individual variation and dynamic response to diet
Minot, S., Sinha, R., Chen, J., Li, H., Keilbaugh, S. A., Wu, G. D., Lewis, J. D., & Bushman, F. D. (2011) · Genome Research · doi:10.1101/gr.122705.111 · Cited by 935 · see citing works
How do site-specific DNA-binding proteins find their targets?
Halford, S. E. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh624 · Cited by 891 · see citing works
The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome
Sebaihia, M., Wren, B. W., Mullany, P. P., Fairweather, N. F., Minton, N. P., Stabler, R. A., Thomson, N. R., Roberts, A. P., Cerdeño-Tárraga, A. M., Wang, H., et al. (2006) · Nature Genetics · doi:10.1038/ng1830 · Cited by 877 · see citing works
The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli
Sapranauskas, R., Gasiūnas, G., Fremaux, C., Barrangou, R., Horvath, P., & Šikšnys, V. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr606 · Cited by 835 · see citing works
Mojica, F. J. M., Díez‐Villaseñor, C., Soria, E., & Juez, G. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01838.x · Cited by 821 · see citing works
Diversity, Activity, and Evolution of CRISPR Loci in Streptococcus thermophilus
Horvath, P., Romero, D. A., Coûté-Monvoisin, A.-C., Richards, M., Deveau, H., Moineau, S., Boyaval, P., Fremaux, C., & Barrangou, R. (2007) · Journal of Bacteriology · doi:10.1128/jb.01415-07 · Cited by 775 · see citing works
Arginine-Mediated RNA Recognition: the Arginine Fork
Calnan, B. J., Tidor, B., Biancalana, S., Hudson, D., & Frankel, A. D. (1991) · Science · doi:10.1126/science.252.5009.1167 · Cited by 746 · see citing works
Selective Silencing of Foreign DNA with Low GC Content by the H-NS Protein in Salmonella
Navarre, W. W., Porwollik, S., Wang, Y., McClelland, M., Rosen, H., Libby, S. J., & Fang, F. C. (2006) · Science · doi:10.1126/science.1128794 · Cited by 727 · see citing works
Semenova, E., Jore, M. M., Datsenko, K. A., Semenova, A., Westra, E. R., Wanner, B. L., John van der, O. O. S. T., Brouns, S. J. J., & Severinov, K. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104144108 · Cited by 726 · see citing works
Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures
Chen, Z., Yang, H., & Pavletich, N. P. (2008) · Nature · doi:10.1038/nature06971 · Cited by 720 · see citing works
Sequence- and Structure-Specific RNA Processing by a CRISPR Endonuclease
Haurwitz, R. E., Jínek, M., Wiedenheft, B., Zhou, K., & Doudna, J. A. (2010) · Science · doi:10.1126/science.1192272 · Cited by 710 · see citing works
Nucleases: diversity of structure, function and mechanism
Yang, W. (2011) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583510000181 · Cited by 692 · see citing works
Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli
Yosef, I., Goren, M. G., & Qimron, U. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks216 · Cited by 680 · see citing works
Explaining Microbial Population Genomics through Phage Predation
Rodriguez-Valera, F., Martin-Cuadrado, A.-B., Rodriguez-Brito, B., Pašić, L., Thingstad, T. F., Rohwer, F., & Mira, A. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2235 · Cited by 663 · see citing works
Self versus non-self discrimination during CRISPR RNA-directed immunity
Marraffini, L. A., & Sontheimer, E. J. (2010) · Nature · doi:10.1038/nature08703 · Cited by 642 · see citing works
Metagenomics: DNA sequencing of environmental samples
Green, S., & Rubin, E. M. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1709 · Cited by 631 · see citing works
CRISPR/Cas System and Its Role in Phage-Bacteria Interactions
Deveau, H., Garneau, J. E., & Moineau, S. (2010) · Annual Review of Microbiology · doi:10.1146/annurev.micro.112408.134123 · Cited by 624 · see citing works
Bacteriophages: Biology and Applications
Silver, S. D., & Baylor, M. B. (2006) · Microbe Magazine · doi:10.1128/microbe.1.151.1 · Cited by 576 · see citing works
Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system
Datsenko, K. A., Pougach, K., Tikhonov, A., Wanner, B. L., Severinov, K., & Semenova, E. (2012) · Nature Communications · doi:10.1038/ncomms1937 · Cited by 569 · see citing works
Structural basis for CRISPR RNA-guided DNA recognition by Cascade
Jore, M. M., Lundgren, M., van Duijn, E., Bultema, J. B., Westra, E. R., Waghmare, S. P., Wiedenheft, B., Pul, Ü., Wurm, R., Wagner, R., et al. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2019 · Cited by 557 · see citing works
Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotesPreprint
Carte, J. M., Wang, R., Li, H., Terns, R. M., & Terns, M. P. (2008) · Genes & Development · doi:10.1101/gad.1742908 · Cited by 551 · see citing works
The phage‐host arms race: Shaping the evolution of microbes
Stern, A., & Sorek, R. (2010) · BioEssays · doi:10.1002/bies.201000071 · Cited by 527 · see citing works
Westra, E. R., van Erp, P. B. G., Künne, T., Wong, S. P., Staals, R. H. J., Seegers, C. L. C., Bollen, S., Jore, M. M., Semenova, E., Severinov, K., et al. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.03.018 · Cited by 511 · see citing works
Phage as agents of lateral gene transfer
Canchaya, C. A., Fournous, G., Chibani-Chennoufi, S., Dillmann, M.-L., & Brüssow, H. (2003) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(03)00086-9 · Cited by 503 · see citing works
Bacteria-Phage Antagonistic Coevolution in Soil
Gómez, P., & Buckling, A. G. J. (2011) · Science · doi:10.1126/science.1198767 · Cited by 492 · see citing works
Virus Population Dynamics and Acquired Virus Resistance in Natural Microbial Communities
Andersson, A. F., & Banfield, J. F. (2008) · Science · doi:10.1126/science.1157358 · Cited by 486 · see citing works
Wiedenheft, B., van Duijn, E., Bultema, J. B., Waghmare, S. P., Zhou, K., Barendregt, A., Westphal, W., Heck, A. J. R., Boekema, E. J., Dickman, M. J., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102716108 · Cited by 449 · see citing works
Evolutionary conservation of sequence and secondary structures in CRISPR repeats
Kunin, V., Sorek, R., & Hugenholtz, P. (2007) · Genome biology · doi:10.1186/gb-2007-8-4-r61 · Cited by 449 · see citing works
Cas3 is a single‐stranded DNA nuclease and ATP‐dependent helicase in the CRISPR/Cas immune system
Šinkūnas, T., Gasiūnas, G., Fremaux, C., Barrangou, R., Horvath, P., & Šikšnys, V. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.41 · Cited by 441 · see citing works
Multidrug-Resistant Enterococci Lack CRISPR- cas
Palmer, K. L., & Gilmore, M. S. (2010) · mBio · doi:10.1128/mbio.00227-10 · Cited by 441 · see citing works
Structures of the RNA-guided surveillance complex from a bacterial immune system
Wiedenheft, B., Lander, G. C., Zhou, K., Jore, M. M., Brouns, S. J. J., John van der, O. O. S. T., Doudna, J. A., & Nogales, E. (2011) · Nature · doi:10.1038/nature10402 · Cited by 398 · see citing works
Self-targeting by CRISPR: gene regulation or autoimmunity?
Stern, A., Keren, L., Wurtzel, O., Amitai, G., & Sorek, R. (2010) · Trends in Genetics · doi:10.1016/j.tig.2010.05.008 · Cited by 384 · see citing works
CRISPR Interference Directs Strand Specific Spacer Acquisition
Swarts, D. C., Mosterd, C., van Passel, M. W. J., & Brouns, S. J. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035888 · Cited by 378 · see citing works
A single-base resolution map of an archaeal transcriptomePreprint
Wurtzel, O., Sapra, R., Chen, F., Zhu, Y., Simmons, B. A., & Sorek, R. (2009) · Genome Research · doi:10.1101/gr.100396.109 · Cited by 356 · see citing works
Godde, J. S., & Bickerton, A. (2006) · Journal of Molecular Evolution · doi:10.1007/s00239-005-0223-z · Cited by 339 · see citing works
Tang, T., Bachellerie, J., Rozhdestvensky, T. S., Bortolin‐Cavaillé, M., Huber, H., Drungowski, M., Elge, T., Brosius, J., & Hüttenhofer, A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.112047299 · Cited by 337 · see citing works
Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses
Tyson, G. W., & Banfield, J. F. (2007) · Environmental Microbiology · doi:10.1111/j.1462-2920.2007.01444.x · Cited by 321 · see citing works
Navarre, W. W., McClelland, M., Libby, S. J., & Fang, F. C. (2007) · Genes & Development · doi:10.1101/gad.1543107 · Cited by 310 · see citing works
Makarova, K. S., Wolf, Y. I., John van der, O. O. S. T., & Koonin, E. V. (2009) · Biology Direct · doi:10.1186/1745-6150-4-29 · Cited by 305 · see citing works
Genomic island variability facilitates Prochlorococcus–virus coexistence
Avrani, S., Wurtzel, O., Sharon, I., Sorek, R., & Lindell, D. (2011) · Nature · doi:10.1038/nature10172 · Cited by 304 · see citing works
Hale, C. R., Majumdar, S., Elmore, J. R., Pfister, N. T., Compton, M. M., Olson, S., Resch, A. M., Glover, C. V. C., Graveley, B. R., Terns, R. M., et al. (2012) · Molecular Cell · doi:10.1016/j.molcel.2011.10.023 · Cited by 294 · see citing works
Structure and Mechanism of the CMR Complex for CRISPR-Mediated Antiviral Immunity
Zhang, J., Rouillon, C., Kerou, M., Reeks, J., Brügger, K., Graham, S., Reimann, J., Cannone, G., Liu, H., Albers, S., et al. (2012) · Molecular Cell · doi:10.1016/j.molcel.2011.12.013 · Cited by 292 · see citing works
Identification and characterization of E. coli CRISPR‐cas promoters and their silencing by H‐NS
Pul, Ü., Wurm, R., Arslan, Z., Geißen, R., Hofmann, N., & Wagner, R. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07073.x · Cited by 286 · see citing works
The CRISPRs, They Are A-Changin': How Prokaryotes Generate Adaptive Immunity
Westra, E. R., Swarts, D. C., Staals, R. H. J., Jore, M. M., Brouns, S. J. J., & John van der, O. O. S. T. (2012) · Annual Review of Genetics · doi:10.1146/annurev-genet-110711-155447 · Cited by 278 · see citing works
Cady, K. C., Bondy-Denomy, J., Heussler, G. E., Davidson, A. R., & O’Toole, G. A. (2012) · Journal of Bacteriology · doi:10.1128/jb.01184-12 · Cited by 274 · see citing works
Lang, B., Blot, N., Bouffartigues, E., Buckle, M., Geertz, M., Gualerzi, C. O., Mavathur, R. N., Muskhelishvili, G., Pon, C. L., Rimsky, S., et al. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm712 · Cited by 269 · see citing works
A dual function of the CRISPR–Cas system in bacterial antivirus immunity and DNA repair
Babu, M., Beloglazova, N. G., Flick, R., Graham, C., Skarina, T., Nocek, B. P., Gagarinova, A. G., Pogoutse, O., Brown, G., Binkowski, A., et al. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07465.x · Cited by 260 · see citing works
Wiedenheft, B., Zhou, K., Jínek, M., Coyle, S. M., Ma, W., & Doudna, J. A. (2009) · Structure · doi:10.1016/j.str.2009.03.019 · Cited by 256 · see citing works
Bouffartigues, E., Buckle, M., Badaut, C., TRAVERS, A. A., & Rimsky, S. (2007) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1233 · Cited by 251 · see citing works
Westra, E. R., Pul, Ü., Heidrich, N., Jore, M. M., Lundgren, M., Stratmann, T., Wurm, R., Raine, A., Mescher, M., van Heereveld, L., et al. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07315.x · Cited by 243 · see citing works
Mechanism of Foreign DNA Selection in a Bacterial Adaptive Immune System
Sashital, D. G., Wiedenheft, B., & Doudna, J. A. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.03.020 · Cited by 238 · see citing works
Prokaryotic silencing (psi)RNAs inPyrococcus furiosus
Hale, C. R., Kleppe, K. L., Terns, R. M., & Terns, M. P. (2008) · RNA · doi:10.1261/rna.1246808 · Cited by 230 · see citing works
A divalent switch drives H-NS/DNA-binding conformations between stiffening and bridging modesPreprint
Liu, Y., Chen, H., Kenney, L. J., & Yan, J. (2010) · Genes & Development · doi:10.1101/gad.1883510 · Cited by 229 · see citing works
Gudbergsdóttir, S. R., Deng, L., Chen, Z., Jensen, J. V. K., Jensen, L. R., She, Q., & Garrett, R. A. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07452.x · Cited by 228 · see citing works
Transcription, processing and function of CRISPR cassettes in Escherichia coli
Pougach, K., Semenova, E., Bogdanova, E. S., Datsenko, K. A., Djordjević, M., Wanner, B. L., & Severinov, K. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07265.x · Cited by 228 · see citing works
Lillestøl, R., Shah, S. A., Brügger, K., Redder, P., Phan, H., Christiansen, J., & Garrett, R. A. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06641.x · Cited by 215 · see citing works
CRISPR targeting reveals a reservoir of common phages associated with the human gut microbiomePreprint
Stern, A., Mick, E., Tirosh, I., Sagy, O., & Sorek, R. (2012) · Genome Research · doi:10.1101/gr.138297.112 · Cited by 212 · see citing works
Nam, K. H., Haitjema, C. H., Liu, X., Ding, F., Wang, H., DeLisa, M. P., & Ke, A. (2012) · Structure · doi:10.1016/j.str.2012.06.016 · Cited by 210 · see citing works
Tang, T., Polacek, N., Żywicki, M., Huber, H., Brügger, K., Garrett, R. A., Bachellerie, J., & Hüttenhofer, A. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04428.x · Cited by 210 · see citing works
Lintner, N. G., Kerou, M., Brumfield, S. K., Graham, S., Liu, H., Naismith, J. H., Sdano, M. A., Peng, N., She, Q., Copié, V., et al. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.238485 · Cited by 201 · see citing works
Beloglazova, N. G., Brown, G., Zimmerman, M. D., Proudfoot, M., Makarova, K. S., Kudritska, M., Kochinyan, S., Wang, S., Chruszcz, M., Minor, W., et al. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m803225200 · Cited by 200 · see citing works
Hatoum-Aslan, A., Maniv, I., & Marraffini, L. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1112832108 · Cited by 199 · see citing works
CRISPR: New Horizons in Phage Resistance and Strain Identification
Barrangou, R., & Horvath, P. (2012) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-022811-101134 · Cited by 198 · see citing works
Structure of a DNA Glycosylase Searching for Lesions
Banerjee, A., Santos, W. L., & Verdine, G. L. (2006) · Science · doi:10.1126/science.1120288 · Cited by 194 · see citing works
Diversity of CRISPR loci in Escherichia coli
Díez‐Villaseñor, C., Almendros, C., García‐Martínez, J., & Mojica, F. J. M. (2010) · Microbiology · doi:10.1099/mic.0.036046-0 · Cited by 194 · see citing works
The viriosphere, diversity, and genetic exchange within phage communities
Hambly, E., & Suttle, C. A. (2005) · Current Opinion in Microbiology · doi:10.1016/j.mib.2005.06.005 · Cited by 194 · see citing works
Denef, V. J., Kalnejais, L. H., Mueller, R., Wilmes, P., Baker, B. J., Thomas, B. C., VerBerkmoes, N. C., Hettich, R. L., & Banfield, J. F. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907041107 · Cited by 183 · see citing works
An RNA-induced conformational change required for CRISPR RNA cleavage by the endoribonuclease Cse3
Sashital, D. G., Jínek, M., & Doudna, J. A. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2043 · Cited by 183 · see citing works
Local Adaptation of Bacteriophages to Their Bacterial Hosts in Soil
Vos, M., Birkett, P. J., Birch, E., Griffiths, R. I., & Buckling, A. G. J. (2009) · Science · doi:10.1126/science.1174173 · Cited by 180 · see citing works
Brüssow, H. (2001) · Annual Review of Microbiology · doi:10.1146/annurev.micro.55.1.283 · Cited by 180 · see citing works
Viral biogeography revealed by signatures in Sulfolobus islandicus genomes
Held, N. L., & Whitaker, R. J. (2009) · Environmental Microbiology · doi:10.1111/j.1462-2920.2008.01784.x · Cited by 173 · see citing works
Interaction of the Cas6 Riboendonuclease with CRISPR RNAs: Recognition and Cleavage
Wang, R., Preamplume, G., Terns, M. P., Terns, R. M., & Li, H. (2011) · Structure · doi:10.1016/j.str.2010.11.014 · Cited by 171 · see citing works
Heidelberg, J. F., Nelson, W. C., Schoenfeld, T. W., & Bhaya, D. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004169 · Cited by 167 · see citing works
Recognition and maturation of effector RNAs in a CRISPR interference pathway
Gesner, E. M., Schellenberg, M. J., Garside, E. L., George, M. M., & MacMillan, A. M. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2042 · Cited by 162 · see citing works
Mechanism of substrate selection by a highly specific CRISPR endoribonuclease
Sternberg, S. H., Haurwitz, R. E., & Doudna, J. A. (2012) · RNA · doi:10.1261/rna.030882.111 · Cited by 153 · see citing works
Biochemical Bases for the Antimetabolite Action of l -Serine Hydroxamate
Tosa, T., & Pizer, L. I. (1971) · Journal of Bacteriology · doi:10.1128/jb.106.3.972-982.1971 · Cited by 148 · see citing works
Binding and cleavage of CRISPR RNA by Cas6
Carte, J. M., Pfister, N. T., Compton, M. M., Terns, R. M., & Terns, M. P. (2010) · RNA · doi:10.1261/rna.2230110 · Cited by 148 · see citing works
Diverse CRISPRs Evolving in Human Microbiomes
Rho, M., Wu, Y., Tang, H., Doak, T. G., & Ye, Y. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002441 · Cited by 146 · see citing works
Protein motion from non‐specific to specific DNA by three‐dimensional routes aided by supercoiling
Gowers, D. M., & Halford, S. E. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg125 · Cited by 143 · see citing works
Persisting Viral Sequences Shape Microbial CRISPR-based Immunity
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. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002475 · Cited by 143 · see citing works
Structure and activity of the Cas3 HD nuclease MJ0384, an effector enzyme of the CRISPR interference
Beloglazova, N. G., Petit, P., Flick, R., Brown, G., Savchenko, A. V., & Yakunin, A. F. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.377 · Cited by 142 · see citing works
CRISPI: a CRISPR interactive database
Rousseau, C., Gonnet, M., Romancer, M. L., & Nicolas, J. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp586 · Cited by 135 · see citing works
Envelope stress is a trigger of CRISPR RNA-mediated DNA silencing in Escherichia coli
Pérez-Rodríguez, R., Haitjema, C. H., Huang, Q., Nam, K. H., Bernardis, S., Ke, A., & DeLisa, M. P. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07482.x · Cited by 132 · see citing works
Low Species Barriers in Halophilic Archaea and the Formation of Recombinant Hybrids
Naor, A., Lapierre, P., Mevarech, M., Papke, R. T., & Gophna, U. (2012) · Current Biology · doi:10.1016/j.cub.2012.05.056 · Cited by 131 · see citing works
Transcription Profile of Thermus thermophilus CRISPR Systems after Phage Infection
Agari, Y., Sakamoto, K., Tamakoshi, M., Oshima, T., Kuramitsu, S., & Shinkai, A. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.10.057 · Cited by 127 · see citing works
Bolduc, B., Shaughnessy, D. P., Wolf, Y. I., Koonin, E. V., Roberto, F. F., & Young, M. (2012) · Journal of Virology · doi:10.1128/jvi.07196-11 · Cited by 127 · see citing works
The CRISPR Associated Protein Cas4 Is a 5′ to 3′ DNA Exonuclease with an Iron-Sulfur Cluster
Zhang, J., Kasciukovic, T., & White, M. F. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047232 · Cited by 126 · see citing works
Levin, B. R. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001171 · Cited by 125 · see citing works
Mulepati, S., & Bailey, S. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.270017 · Cited by 123 · see citing works
Bikard, D., & Marraffini, L. A. (2011) · Current Opinion in Immunology · doi:10.1016/j.coi.2011.10.005 · Cited by 119 · see citing works
Diversity-generating retroelements
Medhekar, B., & Miller, J. F. (2007) · Current Opinion in Microbiology · doi:10.1016/j.mib.2007.06.004 · Cited by 118 · see citing works
Responses of hyperthermophilic crenarchaea to UV irradiation
Götz, D., Paytubi, S., Munro, S., Lundgren, M., Bernander, R., & White, M. F. (2007) · Genome biology · doi:10.1186/gb-2007-8-10-r220 · Cited by 118 · see citing works
CRISPR Associated Diversity within a Population of Sulfolobus islandicus
Held, N. L., Herrera, A., Cadillo‐Quiroz, H., & Whitaker, R. J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012988 · Cited by 116 · see citing works
van der Ploeg, J. R. (2009) · Microbiology · doi:10.1099/mic.0.027508-0 · Cited by 115 · see citing works
Pride, D. T., Sun, C. L., Salzman, J., Rao, N., Loomer, P. M., Armitage, G. C., Banfield, J. F., & Relman, D. A. (2010) · Genome Research · doi:10.1101/gr.111732.110 · Cited by 110 · see citing works
Plagens, A., Tjaden, B., Hagemann, A. R., Randau, L., & Hensel, R. (2012) · Journal of Bacteriology · doi:10.1128/jb.00206-12 · Cited by 109 · see citing works
Medina-Aparicio, L., Rebollar-Flores, J. E., Gallego-Hernández, A. L., Vázquez, A., Olvera, L., Gutiérrez-Ríos, R.-M., Calva, E., & Hernández-Lucas, I. (2011) · Journal of Bacteriology · doi:10.1128/jb.01480-10 · Cited by 106 · see citing works
Childs, L. M., Held, N. L., Young, M., Whitaker, R. J., & Weitz, J. S. (2012) · Evolution · doi:10.1111/j.1558-5646.2012.01595.x · Cited by 100 · see citing works
Csy4 relies on an unusual catalytic dyad to position and cleave CRISPR RNA
Haurwitz, R. E., Sternberg, S. H., & Doudna, J. A. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.107 · Cited by 99 · see citing works
Hernández-Lucas, I., Gallego-Hernández, A. L., Encarnación‐Guevara, S., Fernández‐Mora, M., Martínez-Batallar, Á. G., Salgado, H., Oropeza, R., & Calva, E. (2007) · Journal of Bacteriology · doi:10.1128/jb.01649-07 · Cited by 94 · see citing works
Control of Bacteriophages in Industrial Fermentations
Moineau, S., & Levesque, C. M. (2004) · CRC Press eBooks · doi:10.1201/9780203491751.ch10 · Cited by 89 · see citing works
Young, J. C., Dill, B. D., Pan, C., Hettich, R. L., Banfield, J. F., Shah, M. B., Fremaux, C., Horvath, P., Barrangou, R., & VerBerkmoes, N. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038077 · Cited by 88 · see citing works
Lintner, N. G., Frankel, K. A., Tsutakawa, S. E., Alsbury, D. L., Copié, V., Young, M., Tainer, J. A., & Lawrence, C. M. (2010) · Journal of Molecular Biology · doi:10.1016/j.jmb.2010.11.019 · Cited by 80 · see citing works
Williams, E., Lowe, T. M., Savas, J. N., & DiRuggiero, J. (2006) · Extremophiles · doi:10.1007/s00792-006-0002-9 · Cited by 79 · see citing works
Ebihara, A., Yao, M., Masui, R., Tanaka, I., Yokoyama, S., & Kuramitsu, S. (2006) · Protein Science · doi:10.1110/ps.062131106 · Cited by 77 · see citing works
Structure of the Cmr2 Subunit of the CRISPR-Cas RNA Silencing Complex
Cocozaki, A. I., Ramia, N. F., Shao, Y., Hale, C. R., Terns, R. M., Terns, M. P., & Li, H. (2012) · Structure · doi:10.1016/j.str.2012.01.018 · Cited by 76 · see citing works
He, J., & Deem, M. W. (2010) · Physical Review Letters · doi:10.1103/physrevlett.105.128102 · Cited by 71 · see citing works
Transcription Activation Mediated by a Cyclic AMP Receptor Protein from Thermus thermophilus HB8
Shinkai, A., Kira, S., Nakagawa, N., Kashihara, A., Kuramitsu, S., & Yokoyama, S. (2007) · Journal of Bacteriology · doi:10.1128/jb.01739-06 · Cited by 69 · see citing works
Characterization of the endonuclease SSO2001 from Sulfolobus solfataricus P2
Han, D., & Krauss, G. (2009) · FEBS Letters · doi:10.1016/j.febslet.2009.01.024 · Cited by 66 · see citing works
Nam, K. H., Kurinov, I. V., & Ke, A. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.256263 · Cited by 59 · see citing works
Target Motifs Affecting Natural Immunity by a Constitutive CRISPR-Cas System in Escherichia coli
Almendros, C., Guzman, N. M., Díez‐Villaseñor, C., García‐Martínez, J., & Mojica, F. J. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050797 · Cited by 59 · see citing works
Sorokin, V. A., Gelfand, M. S., & Artamonova, I. I. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.01985-09 · Cited by 57 · see citing works
Zhu, X. Q., & Ye, K. (2012) · FEBS Letters · doi:10.1016/j.febslet.2012.02.036 · Cited by 55 · see citing works
Strand, K. R., Sun, C., Li, T., Jenney, F. E., Schut, G. J., & Adams, M. W. W. (2010) · Archives of Microbiology · doi:10.1007/s00203-010-0570-z · Cited by 54 · see citing works
Structure of a CRISPR-associated protein Cas2 fromDesulfovibrio vulgaris
Samai, P., Smith, P., & Shuman, S. (2010) · Acta Crystallographica Section F Structural Biology and Crystallization Communications · doi:10.1107/s1744309110039801 · Cited by 52 · see citing works
ppGpp-Dependent leuO Expression in Bacteria under Stress
Fang, M., Majumder, A., Tsai, K.-J., & Wu, H.-Y. (2000) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2000.3440 · Cited by 50 · see citing works
LeuO Expression in Response to Starvation for Branched-chain Amino Acids
Majumder, A., Fang, M., Tsai, K.-J., Ueguchi, C., Mizuno, T., & Wu, H.-Y. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m100945200 · Cited by 43 · see citing works
Cascade-mediated binding and bending of negatively supercoiled DNA
Westra, E. R., Nilges, B. S., van Erp, P. B. G., John van der, O. O. S. T., Dame, R. T., & Brouns, S. J. J. (2012) · RNA Biology · doi:10.4161/rna.21410 · Cited by 42 · see citing works
Bacteriophages as model organisms for virus emergence research
Dennehy, J. J. (2009) · Trends in Microbiology · doi:10.1016/j.tim.2009.07.006 · Cited by 41 · see citing works
DNA nicking by HinP1I endonuclease: bending, base flipping and minor groove expansion
Horton, J. R. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkj484 · Cited by 41 · see citing works
Targeted Bacterial Immunity Buffers Phage Diversity
Haerter, J. O., Trusina, A., & Sneppen, K. (2011) · Journal of Virology · doi:10.1128/jvi.05222-11 · Cited by 40 · see citing works
A genome-wide view of the expression and processing patterns of Thermus thermophilus HB8 CRISPR RNAs
Juranek, S., Eban, T., Altuvia, Y., Brown, M., Morozov, P. S., Tuschl, T., & Margalit, H. (2012) · RNA · doi:10.1261/rna.031468.111 · Cited by 35 · see citing works
The impact of CRISPR repeat sequence on structures of a Cas6 protein–RNA complex
Wang, R., Zheng, H., Preamplume, G., Shao, Y., & Li, H. (2012) · Protein Science · doi:10.1002/pro.2028 · Cited by 33 · see citing works
Koo, Y. J., Jung, D.-K., & Bae, E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033401 · Cited by 33 · see citing works
Mulepati, S., Orr, A., & Bailey, S. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.c112.379503 · Cited by 31 · see citing works
Sakamoto, K., Agari, Y., Agari, K., Yokoyama, S., Kuramitsu, S., & Shinkai, A. (2008) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.22358 · Cited by 28 · see citing works
The mysterious RAMP proteins and their roles in small RNA‐based immunity
Wang, R., & Li, H. (2012) · Protein Science · doi:10.1002/pro.2044 · Cited by 25 · see citing works
The crystal structure of the CRISPR-associated protein Csn2 from Streptococcus agalactiae
Ellinger, P., Arslan, Z., Wurm, R., Tschapek, B., MacKenzie, C. R., Pfeffer, K., Panjikar, S., Wagner, R., Schmitt, L., Gohlke, H., et al. (2012) · Journal of Structural Biology · doi:10.1016/j.jsb.2012.04.006 · Cited by 24 · see citing works
Characterization of the multiple CRISPR loci on Streptomyces linear plasmid pSHK1
Guo, P., Cheng, Q., Xie, P., Fan, Y., Jiang, W., & Qin, Z. (2011) · Acta Biochimica et Biophysica Sinica · doi:10.1093/abbs/gmr052 · Cited by 20 · see citing works
CRISPR adaptive immunity systems of prokaryotes
Pougach, K., Lopatina, A., & Severinov, K. (2012) · Molecular Biology · doi:10.1134/s0026893312020136 · Cited by 6 · see citing works
Dangerous weapons: a cautionary tale of CRISPR defence
Dyall‐Smith, M. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07451.x · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Cpf1 Is a Single RNA-Guided Endonuclease of a Class 2 CRISPR-Cas System
Zetsche, B., Gootenberg, J. S., Abudayyeh, O. O., Slaymaker, I. M., Makarova, K. S., Essletzbichler, P., Volz, S. E., Joung, J., John van der, O. O. S. T., Regev, A., et al. (2015) · Cell · doi:10.1016/j.cell.2015.09.038 · Cited by 4,750 · see citing works
Diversity, classification and evolution of CRISPR-Cas systems
Koonin, E. V., Makarova, K. S., & Zhang, F. (2017) · Current Opinion in Microbiology · doi:10.1016/j.mib.2017.05.008 · Cited by 1,423 · see citing works
Structures of Cas9 endonucleases reveal RNA-mediated conformational activation
Jinek, M., Jiang, F., Taylor, D. W., Sternberg, S. H., Kaya, E., Ma, E., Anders, C., Hauer, M., Zhou, K., Lin, S., et al. (2014) · Science · doi:10.1126/science.1247997 · Cited by 1,230 · see citing works
Principles of genetic circuit design
Brophy, J. A. N., & Voigt, C. A. (2014) · Nature Methods · doi:10.1038/nmeth.2926 · Cited by 934 · see citing works
CRISPR-Cas Systems: Prokaryotes Upgrade to Adaptive Immunity
Barrangou, R., & Marraffini, L. A. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.03.011 · Cited by 907 · see citing works
Genome editing in rice and wheat using the CRISPR/Cas system
Shan, Q., Wang, Y., Li, J., & Gao, C. (2014) · Nature Protocols · doi:10.1038/nprot.2014.157 · Cited by 758 · see citing works
Unravelling the structural and mechanistic basis of CRISPR–Cas systems
John van der, O. O. S. T., Westra, E. R., Jackson, R. N., & Wiedenheft, B. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3279 · Cited by 715 · see citing works
Structures of a CRISPR-Cas9 R-loop complex primed for DNA cleavage
Jiang, F., Taylor, D. W., Chen, J. S., Kornfeld, J. E., Zhou, K., Thompson, A. J., Nogales, E., & Doudna, J. A. (2016) · Science · doi:10.1126/science.aad8282 · Cited by 616 · see citing works
Structural Basis for Guide RNA Processing and Seed-Dependent DNA Targeting by CRISPR-Cas12a
Swarts, D. C., John van der, O. O. S. T., & Jínek, M. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.03.016 · Cited by 615 · see citing works
Belhaj, K., Chaparro‐Garcia, A., Kamoun, S., & Nekrasov, V. (2013) · Plant Methods · doi:10.1186/1746-4811-9-39 · Cited by 582 · see citing works
Genome Engineering with Targetable Nucleases
Carroll, D. (2014) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060713-035418 · Cited by 541 · see citing works
Small RNAs in Bacteria and Archaea
Wagner, E. G. H., & Romby, P. (2015) · Advances in genetics · doi:10.1016/bs.adgen.2015.05.001 · Cited by 516 · see citing works
Origins and evolution of CRISPR-Cas systems
Koonin, E. V., & Makarova, K. S. (2019) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2018.0087 · Cited by 494 · see citing works
Abortive Infection: Bacterial Suicide as an Antiviral Immune Strategy
Lopatina, A., Tal, N., & Sorek, R. (2020) · Annual Review of Virology · doi:10.1146/annurev-virology-011620-040628 · Cited by 482 · see citing works
Current applications and future perspective of CRISPR/Cas9 gene editing in cancer
Wang, S.-W., Gao, C., Zheng, Y.-M., Yi, L., Lu, J.-C., Huang, X.-Y., Cai, J.-B., Zhang, P.-F., Cui, Y.-H., & Ke, A.-W. (2022) · Molecular Cancer · doi:10.1186/s12943-022-01518-8 · Cited by 478 · see citing works
Type III CRISPR–Cas systems produce cyclic oligoadenylate second messengers
Niewoehner, O., Garcia‐Doval, C., Rostøl, J. T., Berk, C., Schwede, F., Bigler, L., Hall, J., Marraffini, L. A., & Jínek, M. (2017) · Nature · doi:10.1038/nature23467 · Cited by 464 · see citing works
Cas1–Cas2 complex formation mediates spacer acquisition during CRISPR–Cas adaptive immunity
Nuñez, J. K., Kranzusch, P. J., Noeske, J., Wright, A. V., Davies, C., & Doudna, J. A. (2014) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2820 · Cited by 458 · see citing works
Programmable Removal of Bacterial Strains by Use of Genome-Targeting CRISPR-Cas Systems
Gomaa, A. A., Klumpe, H. E., Luo, M. L., Selle, K., Barrangou, R., & Beisel, C. L. (2014) · mBio · doi:10.1128/mbio.00928-13 · Cited by 437 · see citing works
The crystal structure of Cpf1 in complex with CRISPR RNA
Dong, D., Ren, K., Qiu, X., Zheng, J., Guo, M., Guan, X., Liu, H., Li, N., Zhang, B., Yang, D.-J., et al. (2016) · Nature · doi:10.1038/nature17944 · Cited by 413 · see citing works
Genome-Editing Technologies: Principles and ApplicationsPreprint
Gaj, T., Sirk, S. J., Shui, S., & Liu, J. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a023754 · Cited by 425 · see citing works
CRISPR–Cas adaptation: insights into the mechanism of action
Amitai, G., & Sorek, R. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2015.14 · Cited by 411 · see citing works
CRISPR adaptation biases explain preference for acquisition of foreign DNA
Levy, A., Goren, M. G., Yosef, I., Auster, O., Manor, M., Amitai, G., Edgar, R., Qimron, U., & Sorek, R. (2015) · Nature · doi:10.1038/nature14302 · Cited by 408 · see citing works
Methodologies for Improving HDR Efficiency
Liu, M.-J., Rehman, S., Tang, X., Gu, K., Fan, Q., Chen, D., & Ma, W. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2018.00691 · Cited by 350 · see citing works
CRISPR/Cas9-mediated targeted mutagenesis in Nicotiana tabacum
Gao, J., Wang, G., Ma, S., Xie, X., Wu, X., Zhang, X., Wu, Y., Zhao, P., & Xia, Q. (2014) · Plant Molecular Biology · doi:10.1007/s11103-014-0263-0 · Cited by 340 · see citing works
Identifying and Visualizing Functional PAM Diversity across CRISPR-Cas Systems
Leenay, R. T., Maksimchuk, K. R., Slotkowski, R., Agrawal, R. N., Gomaa, A. A., Briner, A. E., Barrangou, R., & Beisel, C. L. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.02.031 · Cited by 325 · see citing works
DISARM is a widespread bacterial defence system with broad anti-phage activities
Ofir, G., Melamed, S., Sberro, H., Mukamel, Z., Silverman, S., Yaakov, G., Doron, S., & Sorek, R. (2017) · Nature Microbiology · doi:10.1038/s41564-017-0051-0 · Cited by 333 · see citing works
CRISPRDetect: A flexible algorithm to define CRISPR arrays
Biswas, A., Staals, R. H. J., Morales, S. E., Fineran, P. C., & Brown, C. M. (2016) · BMC Genomics · doi:10.1186/s12864-016-2627-0 · Cited by 332 · see citing works
CRISPR–Cas systems: beyond adaptive immunity
Westra, E. R., Buckling, A., & Fineran, P. C. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3241 · Cited by 322 · see citing works
iSCAN: An RT-LAMP-coupled CRISPR-Cas12 module for rapid, sensitive detection of SARS-CoV-2
Ali, Z., Aman, R. A., Mahas, A., Rao, G. S., Tehseen, M., Maršić, T., Salunke, R. P., Subudhi, A. K., Hala, S. M., Hamdan, S. M., et al. (2020) · Virus Research · doi:10.1016/j.virusres.2020.198129 · Cited by 315 · see citing works
Conditional tolerance of temperate phages via transcription-dependent CRISPR-Cas targeting
Goldberg, G. W., Jiang, W., Bikard, D., & Marraffini, L. A. (2014) · Nature · doi:10.1038/nature13637 · Cited by 284 · see citing works
Contemporary Phage Biology: From Classic Models to New Insights
Ofir, G., & Sorek, R. (2018) · Cell · doi:10.1016/j.cell.2017.10.045 · Cited by 293 · see citing works
Remarkable Mechanisms in Microbes to Resist Phage Infections
Dy, R. L. V., Richter, C., Salmond, G. P. C., & Fineran, P. C. (2014) · Annual Review of Virology · doi:10.1146/annurev-virology-031413-085500 · Cited by 284 · see citing works
CRISPR Crops: Plant Genome Editing Toward Disease Resistance
Langner, T., Kamoun, S., & Belhaj, K. (2018) · Annual Review of Phytopathology · doi:10.1146/annurev-phyto-080417-050158 · Cited by 290 · see citing works
PAM identification by CRISPR-Cas effector complexes: diversified mechanisms and structures
Gleditzsch, D., Pausch, P., Müller-Esparza, H., Özcan, A., Guo, X., Bange, G., & Randau, L. (2018) · RNA Biology · doi:10.1080/15476286.2018.1504546 · Cited by 281 · see citing works
Consequences of Cas9 cleavage in the chromosome of Escherichia coli
Cui, L., & Bikard, D. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw223 · Cited by 266 · see citing works
Degenerate target sites mediate rapid primed CRISPR adaptation
Fineran, P. C., Gerritzen, M. J. H., Diez, M. S., Künne, T., Boekhorst, J., van Hijum, S. A. F. T., Staals, R. H. J., & Brouns, S. J. J. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400071111 · Cited by 267 · see citing works
The Genomic Diversification of the Whole Acinetobacter Genus: Origins, Mechanisms, and Consequences
Touchon, M., Cury, J., Yoon, E.-J., Křížová, L., Cerqueira, G., Murphy, C. I., Feldgarden, M., Wortman, J. R., Clermont, D., Lambert, T., et al. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu225 · Cited by 273 · see citing works
The roles of CRISPR–Cas systems in adaptive immunity and beyond
Barrangou, R. (2015) · Current Opinion in Immunology · doi:10.1016/j.coi.2014.12.008 · Cited by 260 · see citing works
Structural basis of CRISPR–SpyCas9 inhibition by an anti-CRISPR protein
Dong, D., Guo, M., Wang, S., Zhu, Y., Wang, S., Xiong, Z., Yang, J., Xu, Z., & Huang, Z. (2017) · Nature · doi:10.1038/nature22377 · Cited by 255 · see citing works
The Human Gut Phage Community and Its Implications for Health and Disease
Manrique, P., Dills, M., & Young, M. (2017) · Viruses · doi:10.3390/v9060141 · Cited by 253 · see citing works
Cas9-mediated targeting of viral RNA in eukaryotic cells
Price, A. A., Sampson, T. R., Ratner, H. K., Grakoui, A., & Weiss, D. S. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1422340112 · Cited by 252 · see citing works
Crystal structure of the CRISPR RNA–guided surveillance complex from Escherichia coli
Jackson, R. N., Golden, S. M., van Erp, P. B. G., Carter, J. J., Westra, E. R., Brouns, S. J. J., John van der, O. O. S. T., Terwilliger, T. C., Read, R. J., & Wiedenheft, B. (2014) · Science · doi:10.1126/science.1256328 · Cited by 245 · see citing works
Repurposing endogenous type I CRISPR-Cas systems for programmable gene repression
Luo, M. L., Mullis, A. S., Leenay, R. T., & Beisel, C. L. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku971 · Cited by 239 · see citing works
Structure of the Cpf1 endonuclease R-loop complex after target DNA cleavage
Stella, S., Alcón, P., & Montoya, G. (2017) · Nature · doi:10.1038/nature22398 · Cited by 224 · see citing works
Burroughs, A. M., Zhang, D., Schäffer, D. E., Iyer, L. M., & Aravind, L. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1267 · Cited by 237 · see citing works
Zhang, J., Zong, W., Hong, W., Zhang, Z.-T., & Wang, Y. (2018) · Metabolic Engineering · doi:10.1016/j.ymben.2018.03.007 · Cited by 233 · see citing works
Direct observation of DNA target searching and cleavage by CRISPR-Cas12a
Jeon, Y., Choi, Y. H., Jang, Y., Yu, J., Goo, J., Lee, G., Jeong, Y. K., Lee, S. H., Kim, I.-S., Kim, J., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05245-x · Cited by 229 · see citing works
A CRISPR view of developmentPreprint
Harrison, M. M., Jenkins, B., O’Connor-Giles, K. M., & Wildonger, J. (2014) · Genes & Development · doi:10.1101/gad.248252.114 · Cited by 228 · see citing works
Crystal structure of a CRISPR RNA–guided surveillance complex bound to a ssDNA target
Mulepati, S., Heroux, A., & Bailey, S. (2014) · Science · doi:10.1126/science.1256996 · Cited by 225 · see citing works
Principles, Applications, and Biosafety of Plant Genome Editing Using CRISPR-Cas9
El‐Mounadi, K., Morales-Floriano, M. L., & García-Ruíz, H. (2020) · Frontiers in Plant Science · doi:10.3389/fpls.2020.00056 · Cited by 227 · see citing works
The CRISPR Spacer Space Is Dominated by Sequences from Species-Specific Mobilomes
Shmakov, S., Sitnik, V., Makarova, K. S., Wolf, Y. I., Severinov, K., & Koonin, E. V. (2017) · mBio · doi:10.1128/mbio.01397-17 · Cited by 210 · see citing works
Multigene Knockout Utilizing Off-Target Mutations of the CRISPR/Cas9 System in Rice
Endo, M., Mikami, M., & Toki, S. (2014) · Plant and Cell Physiology · doi:10.1093/pcp/pcu154 · Cited by 213 · see citing works
The Revolution Continues: Newly Discovered Systems Expand the CRISPR-Cas Toolkit
Murugan, K., Babu, K., Sundaresan, R., Rajan, R., & Sashital, D. G. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.09.007 · Cited by 204 · see citing works
Structural Plasticity of PAM Recognition by Engineered Variants of the RNA-Guided Endonuclease Cas9
Anders, C., Bargsten, K., & Jinek, M. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.02.020 · Cited by 201 · see citing works
Lau, R., Ye, Q., Birkholz, E. A., Berg, K. R., Patel, L., Mathews, I. T., Watrous, J. D., Ego, K. M., Whiteley, A. T., Lowey, B., et al. (2020) · Molecular Cell · doi:10.1016/j.molcel.2019.12.010 · Cited by 199 · see citing works
DNA Unwinding Is the Primary Determinant of CRISPR-Cas9 Activity
Gong, S., Yu, H. H., Johnson, K. A., & Taylor, D. W. (2018) · Cell Reports · doi:10.1016/j.celrep.2017.12.041 · Cited by 193 · see citing works
Park, J. Y., Moon, B. Y., Park, J. W., Thornton, J. A., Park, Y. H., & Seo, K. S. (2017) · Scientific Reports · doi:10.1038/srep44929 · Cited by 195 · see citing works
Implementation of the CRISPR-Cas9 system in fission yeast
Jacobs, J. Z., Ciccaglione, K. M., Tournier, V., & Zaratiegui, M. (2014) · Nature Communications · doi:10.1038/ncomms6344 · Cited by 190 · see citing works
CARF and WYL domains: ligand-binding regulators of prokaryotic defense systems
Makarova, K. S., Anantharaman, V., Grishin, N. V., Koonin, E. V., & Aravind, L. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2014.00102 · Cited by 171 · see citing works
Richter, C., Dy, R. L. V., McKenzie, R. E., Watson, B. N. J., Taylor, C., Chang, J. T., McNeil, M. B., Staals, R. H. J., & Fineran, P. C. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku527 · Cited by 183 · see citing works
Pyne, M. E., Bruder, M. R., Moo‐Young, M., Chung, D. A., & Chou, C.-H. P. (2016) · Scientific Reports · doi:10.1038/srep25666 · Cited by 175 · see citing works
Evolution of adaptive immunity from transposable elements combined with innate immune systems
Koonin, E. V., & Krupovìč, M. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3859 · Cited by 176 · see citing works
Prykhozhij, S. V., Rajan, V., Gaston, D., & Berman, J. N. (2015) · PLoS ONE · doi:10.1371/journal.pone.0119372 · Cited by 174 · see citing works
The structural biology of CRISPR-Cas systems
Jiang, F., & Doudna, J. A. (2015) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2015.02.002 · Cited by 174 · see citing works
Mobile Genetic Elements and Evolution of CRISPR-Cas Systems: All the Way There and Back
Koonin, E. V., & Makarova, K. S. (2017) · Genome Biology and Evolution · doi:10.1093/gbe/evx192 · Cited by 166 · see citing works
Anti-CRISPRs: Protein Inhibitors of CRISPR-Cas Systems
Davidson, A. R., Lu, W., Stanley, S. Y., Wang, J., Mejdani, M., Trost, C. N., Hicks, B. T., Lee, J., & Sontheimer, E. J. (2020) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-011420-111224 · Cited by 167 · see citing works
Markerless chromosomal gene deletion in Clostridium beijerinckii using CRISPR/Cas9 system
Wang, Y., Zhang, Z.-T., Seo, S.-O., Choi, K., Lu, T., Jin, Y.-S., & Blaschek, H. P. (2015) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2015.02.005 · Cited by 161 · see citing works
Juszczuk‐Kubiak, E. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25052655 · Cited by 162 · see citing works
Shmakov, S., Makarova, K. S., Wolf, Y. I., Severinov, K., & Koonin, E. V. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1803440115 · Cited by 157 · see citing works
Next-Generation Sequencing and Genome Editing in Plant Virology
Hadidi, A., Flores, R., Candresse, T., & Barba, M. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01325 · Cited by 156 · see citing works
Pseudomonas aeruginosa defends against phages through type IV pilus glycosylation
Harvey, H., Bondy‐Denomy, J., Marquis, H., Sztanko, K. M., Davidson, A. R., & Burrows, L. L. (2017) · Nature Microbiology · doi:10.1038/s41564-017-0061-y · Cited by 154 · see citing works
Extensive intra-phylotype diversity in lactobacilli and bifidobacteria from the honeybee gut
Ellegaard, K., Tamarit, D., Javelind, E., Olofsson, T. C., Andersson, S. G. E., & Vásquez, A. (2015) · BMC Genomics · doi:10.1186/s12864-015-1476-6 · Cited by 153 · see citing works
CRISPR-Cas14 is now part of the artillery for gene editing and molecular diagnostic
Aquino‐Jarquín, G. (2019) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2019.03.006 · Cited by 153 · see citing works
Origin and Evolution of Adaptive Immunity
Boehm, T. L. J., & Swann, J. B. (2013) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-022513-114201 · Cited by 144 · see citing works
Initiation of mRNA decay in bacteria
Laalami, S., Zig, L., & Putzer, H. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1472-4 · Cited by 144 · see citing works
Towards application of CRISPR-Cas12a in the design of modern viral DNA detection tools (Review)
Dronina, J., Samukaitė-Bubnienė, U., & Ramanavičius, A. (2022) · Journal of Nanobiotechnology · doi:10.1186/s12951-022-01246-7 · Cited by 144 · see citing works
An anti-CRISPR protein disables type V Cas12a by acetylation
Dong, L., Guan, X., Li, N., Zhang, F., Zhu, Y., Ren, K., Yu, L., Zhou, F., Han, Z., Gao, N., et al. (2019) · Nature Structural & Molecular Biology · doi:10.1038/s41594-019-0206-1 · Cited by 141 · see citing works
CRISPR-Cas-Mediated Phage Resistance Enhances Horizontal Gene Transfer by Transduction
Watson, B. N. J., Staals, R. H. J., & Fineran, P. C. (2018) · mBio · doi:10.1128/mbio.02406-17 · Cited by 140 · see citing works
Cutting it close: CRISPR-associated endoribonuclease structure and function
Hochstrasser, M. L., & Doudna, J. A. (2014) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2014.10.007 · Cited by 135 · see citing works
Mantravadi, P. K., Kalesh, K., Dobson, R. C. J., Hudson, A. O., & Parthasarathy, A. (2019) · Antibiotics · doi:10.3390/antibiotics8010008 · Cited by 141 · see citing works
Paepe, M. D., Hutinet, G., Son, O., Amarir-Bouhram, J., Schbath, S., & Petit, M. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004181 · Cited by 134 · see citing works
Repurposing CRISPR/Cas9 for in situ functional assaysPreprint
Malina, A., Mills, J. R., Cencic, R., Yan, Y., Fraser, J., Nederveen-Schippers, L. M., Paquet, M., Dostie, J., & Pelletier, J. (2013) · Genes & Development · doi:10.1101/gad.227132.113 · Cited by 132 · see citing works
Crystal Structure of the CRISPR-Cas RNA Silencing Cmr Complex Bound to a Target Analog
Osawa, T., Inanaga, H., Sato, C., & Numata, T. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.03.018 · Cited by 131 · see citing works
Structure of an RNA Silencing Complex of the CRISPR-Cas Immune System
Spilman, M. S., Cocozaki, A. I., Hale, C. R., Shao, Y., Ramia, N. F., Terns, R., Terns, M. P., Li, H., & Stagg, S. M. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.09.008 · Cited by 130 · see citing works
Heritable Custom Genomic Modifications in Caenorhabditis elegans via a CRISPR–Cas9 System
Tzur, Y. B., Friedland, A. E., Nadarajan, S., Church, G. M., Calarco, J. A., & Colaiácovo, M. P. (2013) · Genetics · doi:10.1534/genetics.113.156075 · Cited by 126 · see citing works
Structural basis for the endoribonuclease activity of the type III-A CRISPR-associated protein Csm6
Niewoehner, O., & Jínek, M. (2016) · RNA · doi:10.1261/rna.054098.115 · Cited by 127 · see citing works
Xiao, R., Li, Z., Wang, S., Han, R., & Chang, L. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab179 · Cited by 131 · see citing works
Multigene disruption in undomesticated Bacillus subtilis ATCC 6051a using the CRISPR/Cas9 system
Zhang, K., Duan, X., & Wu, J. (2016) · Scientific Reports · doi:10.1038/srep27943 · Cited by 126 · see citing works
Oliva, G., Sahr, T., & Buchrieser, C. (2015) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuv022 · Cited by 125 · see citing works
Detection and characterization of spacer integration intermediates in type I-E CRISPR–Cas system
Arslan, Z., Hermanns, V. D.-B., Wurm, R., Wagner, R., & Pul, Ü. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku510 · Cited by 124 · see citing works
Bonini, A., Poma, N. V., Vivaldi, F. M., Kirchhain, A., Salvo, P., Bottai, D., Tavanti, A., & Francesco, F. D. (2020) · Journal of Pharmaceutical and Biomedical Analysis · doi:10.1016/j.jpba.2020.113645 · Cited by 124 · see citing works
Evolving Ideas on the Origin and Evolution of Flowers: New Perspectives in the Genomic Era
Chanderbali, A. S., Berger, B., Howarth, D. G., Soltis, P. S., & Soltis, P. S. (2016) · Genetics · doi:10.1534/genetics.115.182964 · Cited by 122 · see citing works
Harnessing CRISPR/Cas systems for programmable transcriptional and post-transcriptional regulation
Mahas, A., Stewart, C. N., & Mahfouz, M. M. (2017) · Biotechnology Advances · doi:10.1016/j.biotechadv.2017.11.008 · Cited by 121 · see citing works
Covalent Modification of Bacteriophage T4 DNA Inhibits CRISPR-Cas9
Bryson, A. L., Hwang, Y., Sherrill-Mix, S. A., Wu, G. D., Lewis, J. D., Black, L. W., Clark, T. A., & Bushman, F. D. (2015) · mBio · doi:10.1128/mbio.00648-15 · Cited by 114 · see citing works
Molecular mechanisms of CRISPR-mediated microbial immunity
Gasiūnas, G., Šinkūnas, T., & Šikšnys, V. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1438-6 · Cited by 117 · see citing works
Diversity of CRISPR-Cas immune systems and molecular machines
Barrangou, R. (2015) · Genome biology · doi:10.1186/s13059-015-0816-9 · Cited by 115 · see citing works
The Common Ancestor of Archaea and Eukarya Was Not an Archaeon
Forterre, P. (2013) · Archaea · doi:10.1155/2013/372396 · Cited by 112 · see citing works
Massively Parallel Biophysical Analysis of CRISPR-Cas Complexes on Next Generation Sequencing Chips
Jung, C., Hawkins, J. A., Jones, S. K., Xiao, Y., Rybarski, J. R., Dillard, K. E., Hussmann, J. A., Saifuddin, F. A., Savran, C. A., Ellington, A. D., et al. (2017) · Cell · doi:10.1016/j.cell.2017.05.044 · Cited by 112 · see citing works
Intrinsic sequence specificity of the Cas1 integrase directs new spacer acquisition
Rollie, C., Schneider, S., Brinkmann, A. S., Bolt, E. L., & White, M. F. (2015) · eLife · doi:10.7554/elife.08716 · Cited by 111 · see citing works
Farasat, I., & Salis, H. M. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004724 · Cited by 110 · see citing works
- Authors
- Sorek, R., Lawrence, C. M., & Wiedenheft, B.
- Affiliations
- Weizmann Institute of Science (IL)
- Montana State University (US)
- Venue
- Annual Review of Biochemistry
- Publisher
- Annual Reviews
- Published
- 2013-06-02
- Volume
- 82
- Issue
- 1
- Pages
- 237-266
- ISSN
- 0066-4154 (ISSN-L)
- 1545-4509
- OpenAlex
- W2131157113
- Cited by
- 668
- References
- 158
- Citations by year
- 2026: 12 · 2025: 32 · 2024: 52 · 2023: 54 · 2022: 46 · 2021: 44 · 2020: 58 · 2019: 42 · 2018: 46 · 2017: 59 · 2016: 53 · 2015: 67 · 2014: 79 · 2013: 23
- FWCI
- 6.96
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Annual Review of Biochemistry (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (0628732, 0920312)
- Leona M. and Harry B. Helmsley Charitable Trust
- Deutsche Forschungsgemeinschaft
- Israel Science Foundation (1303/12)
- National Institutes of Health
- National Institute of General Medical Sciences (GM-103500, R01GM108888, P20GM103500)
- National Center for Research Resources
- FP7 Ideas: European Research Council (260432)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Physical Sciences › Environmental Science › Ecology › Bacteriophages and microbial interactions
- Keywords
- CRISPR, adaptive immunity, bacteria, archaea, small RNA, autoimmunity, immune evasion, evolutionary implications, ecological implications
- MeSH terms
- Archaea, Bacteria, RNA, Bacterial, Signal Transduction, RNA, Archaeal, Inverted Repeat Sequences, Adaptive Immunity
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review