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Crystal Structure of Cas9 in Complex with Guide RNA and Target DNA
Open accessAbstract
The CRISPR-associated endonuclease Cas9 can be targeted to specific genomic loci by single guide RNAs (sgRNAs). Here, we report the crystal structure of Streptococcus pyogenes Cas9 in complex with sgRNA and its target DNA at 2.5 Å resolution. The structure revealed a bilobed architecture composed of target recognition and nuclease lobes, accommodating the sgRNA:DNA heteroduplex in a positively charged groove at their interface. Whereas the recognition lobe is essential for binding sgRNA and DNA, the nuclease lobe contains the HNH and RuvC nuclease domains, which are properly positioned for cleavage of the complementary and noncomplementary strands of the target DNA, respectively. The nuclease lobe also contains a carboxyl-terminal domain responsible for the interaction with the protospacer adjacent motif (PAM). This high-resolution structure and accompanying functional analyses have revealed the molecular mechanism of RNA-guided DNA targeting by Cas9, thus paving the way for the rational design of new, versatile genome-editing technologies.
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“Upon binding of Streptococcus pyogenes Cas9 (SpCas9) to the target site, a stable strand separation is maintained through two kinds of interactions: the binding of gRNA to the target strand, and a positively-charged groove resulting from the unspecific interaction of both HNH and RuvC domains with the negatively-charged non-target strand [36].”
From CRISPR-Cas: Converting A Bacterial Defence Mechanism into A State-of-the-Art Genetic Manipulation Tool (2019) · cites this paper as [36]
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“tracrRNA is complementary to the repeat sequence and contains 3 stem-loop hairpin structures [35,36].”
From CRISPR-Cas: Converting A Bacterial Defence Mechanism into A State-of-the-Art Genetic Manipulation Tool (2019) · cites this paper as [36]
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“The structure that came out of the laboratory of Jennifer Doudna was of an apo-protein (PDBe ID 4cmp, PDBe DOI: 10.2210/pdb4cmp/pdb), while the research group of Osamu Nureki (University of Tokyo, Japan) succeeded in crystallising the protein in a complex with a “guide”-RNA and “target”-DNA (PDBe ID 4oo8, PDBe DOI: 10.2210/pdb4oo8/pdb).”
From CRISPR–Cas9: A History of Its Discovery and Ethical Considerations of Its Use in Genome Editing (2022) · cites this paper as [40]
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In the citing paper
“The key structures of the nuclease lobe of SpCas9 are 2 domains: HNH and RuvC, each of them cleaves one of the target DNA strands.”
From CRISPR–Cas9: A History of Its Discovery and Ethical Considerations of Its Use in Genome Editing (2022) · cites this paper as [40]
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“For example, SpCas9-NG shows reduced editing efficiency on 5′-NGC-3′ PAM targets and tends to increase off-target activity (Nishimasu et al., 2014).”
From Emerging applications of gene editing technologies for the development of climate-resilient crops (2025) · cites this paper as Nishimasu et al., 2014
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In the citing paper
“Crystal structures revealed that the Cas9 protein is spatially divided into 2 lobes: a target recognition lobe and a nuclease lobe, with the guide RNA and target DNA occupying the positively charged groove at their interface.”
From CRISPR–Cas9: A History of Its Discovery and Ethical Considerations of Its Use in Genome Editing (2022) · cites this paper as [40]
In the citing paper
“Attempts to obtain detailed information about the structure of this protein resulted in the first two crystallographic studies being published almost simultaneously: in February 2014 two crystal structures of Cas9 appeared in the database PDBe (“Protein Data Bank in Europe”), and the accompanying articles were published in the journals Nature and Cell [39, 40].”
From CRISPR–Cas9: A History of Its Discovery and Ethical Considerations of Its Use in Genome Editing (2022) · cites this paper as [40]
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“These, as well as many subsequent studies, used the Cas9 protein from S. pyogenes, SpCas9, which consists of 1368 amino acids and is a multidomain and multifunctional endonuclease.”
From CRISPR–Cas9: A History of Its Discovery and Ethical Considerations of Its Use in Genome Editing (2022) · cites this paper as [40]
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Lei, C., Li, S., Liu, J.-K., Zheng, X., Zhao, G., & Wang, J. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx018 · Cited by 66
Zhao, C., Shu, X., & Sun, B. (2017) · Applied and Environmental Microbiology · doi:10.1128/aem.00291-17 · Cited by 65
Creating cell and animal models of human disease by genome editing using CRISPR/Cas9
Zarei, A., Razban, V., Hosseini, S. E., & Tabei, K. (2019) · The Journal of Gene Medicine · doi:10.1002/jgm.3082 · Cited by 68
Unified energetics analysis unravels SpCas9 cleavage activity for optimal gRNA design
Zhang, D., Hurst, T., Duan, D., & Chen, S. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820523116 · Cited by 63
Maggio, I., Zittersteijn, H. A., Wang, Q., Liu, J., Janssen, J. M., Ojeda, I. T., van der Maarel, S. M., Lankester, A. C., Hoeben, R. C., & Gonçalves, M. A. F. V. (2020) · Gene Therapy · doi:10.1038/s41434-019-0119-y · Cited by 66
Structural insights into a high fidelity variant of SpCas9
Guo, M., Ren, K., Zhu, Y., Tang, Z., Wang, Y., Zhang, B., & Huang, Z. (2019) · Cell Research · doi:10.1038/s41422-018-0131-6 · Cited by 65
Genome Editing in Agriculture: Technical and Practical Considerations
Jansing, J., Schiermeyer, A., Schillberg, S., Fischer, R., & Bortesi, L. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20122888 · Cited by 66
Application of CRISPR/Cas9 genome editing to the study and treatment of disease
Pellagatti, A., Dolatshad, H., Valletta, S., & Boultwood, J. (2015) · Archives of Toxicology · doi:10.1007/s00204-015-1504-y · Cited by 65
Structure and Dynamics of Cas9 HNH Domain Catalytic State
Zuo, Z., & Liu, J. (2017) · Scientific Reports · doi:10.1038/s41598-017-17578-6 · Cited by 68
DNA methylation and de-methylation using hybrid site-targeting proteins
Lei, Y., Huang, Y., & Goodell, M. A. (2018) · Genome biology · doi:10.1186/s13059-018-1566-2 · Cited by 67
Engineer chimeric Cas9 to expand PAM recognition based on evolutionary information
Ma, D., Xu, Z., Zhang, Z., Chen, X., Zeng, X., Zhang, Y., Deng, T., Ren, M., Sun, Z., Jiang, R., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-08395-8 · Cited by 66
Taemaitree, L., Shivalingam, A., El-Sagheer, A. H., & Brown, T. P. (2019) · Nature Communications · doi:10.1038/s41467-019-09600-4 · Cited by 61
Reprogrammed tracrRNAs enable repurposing of RNAs as crRNAs and sequence-specific RNA biosensors
Liu, Y., Pinto, F., Wan, X., Yang, Z., Peng, S., Li, M., Cooper, J. M., Xie, Z., French, C. E., & Wang, B. (2022) · Nature Communications · doi:10.1038/s41467-022-29604-x · Cited by 66
Deep mutational scanning of S. pyogenes Cas9 reveals important functional domains
Spencer, J. M., & Zhang, X. (2017) · Scientific Reports · doi:10.1038/s41598-017-17081-y · Cited by 65
Genome editing technologies and their applications in crop improvement
Mishra, R., & Zhao, K. (2018) · Plant Biotechnology Reports · doi:10.1007/s11816-018-0472-0 · Cited by 72
Kim, S. M., Shin, S. C., Kim, E. E., Kim, S., Park, K., Oh, S. J., & Jang, M. (2018) · ACS Nano · doi:10.1021/acsnano.8b01670 · Cited by 63
Endogenous CRISPR-Cas System-Based Genome Editing and Antimicrobials: Review and Prospects
Li, Y., & Peng, N. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.02471 · Cited by 65
Functional Features and Current Applications of the RNA‐Targeting Type VI CRISPR‐Cas Systems
Perčulija, V., Lin, J., Zhang, B., & Ouyang, S. (2021) · Advanced Science · doi:10.1002/advs.202004685 · Cited by 60
Sniper2L is a high-fidelity Cas9 variant with high activity
Kim, Y.-H., Kim, N., Okafor, I. C., Choi, S.-C., Min, S., Lee, J., Bae, S.-M., Choi, K., Choi, J., Harihar, V., et al. (2023) · Nature Chemical Biology · doi:10.1038/s41589-023-01279-5 · Cited by 70
Application of CRISPR/Cas9 for biomedical discoveries
Riordan, S. M., Heruth, D. P., Zhang, L. Q., & Ye, S. Q. (2015) · Cell & Bioscience · doi:10.1186/s13578-015-0027-9 · Cited by 66
Genome Editing with CRISPR-Cas9: Can It Get Any Better?
Haeussler, M., & Concordet, J. (2016) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2016.04.008 · Cited by 65
CRISPR/Cas9: a double-edged sword when used to combat HIV infection
Chen, L., Wainberg, M. A., Das, A. T., & Berkhout, B. (2016) · Retrovirology · doi:10.1186/s12977-016-0270-0 · Cited by 62
Barakate, A., & Stephens, J. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.00765 · Cited by 64
CRISPR-Cas9 gene editing: Delivery aspects and therapeutic potential
Blenke, E. O., Evers, M. J. W., Mastrobattista, E., & John van der, O. O. S. T. (2016) · Journal of Controlled Release · doi:10.1016/j.jconrel.2016.08.002 · Cited by 63
Efficient In Vivo Liver-Directed Gene Editing Using CRISPR/Cas9
Singh, K., Evens, H., Nair, N., Rincón, M. Y., Sarcar, S., Samara-Kuko, E., Chuah, M., & VandenDriessche, T. (2018) · Molecular Therapy · doi:10.1016/j.ymthe.2018.02.023 · Cited by 63
RNase H As Gene Modifier, Driver of Evolution and Antiviral Defense
Moelling, K., Broecker, F., Russo, G., & Sunagawa, S. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01745 · Cited by 62
Advances in Genome Editing and Application to the Generation of Genetically Modified Rat Models
Chenouard, V., Remy, S., Tesson, L., Ménoret, S., Ouisse, L.-H., Cherifi, Y., & Anegon, I. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.615491 · Cited by 57
Metadata
- Authors
- Nishimasu, H., Ran, F. A., Hsu, P. D., Konermann, S., Shehata, S. I., Dohmae, N., Ishitani, R., Zhang, F., & Nureki, O.
- Affiliations
- Japan Science and Technology Agency (JP)
- Broad Institute (US)
- RIKEN (JP)
- The University of Tokyo (JP)
- Corresponding author
- Zhang, Feng
- Nureki, Osamu
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2014-02
- Volume
- 156
- Issue
- 5
- Pages
- 935-949
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC4139937
- OpenAlex
- W2107959600
- Cited by
- 2,306
- References
- 77
- Citations by year
- 2026: 130 · 2025: 193 · 2024: 221 · 2023: 177 · 2022: 229 · 2021: 218 · 2020: 215 · 2019: 212 · 2018: 191 · 2017: 193 · 2016: 149 · 2015: 93 · 2014: 80
- FWCI
- 70.34
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
- eScholarship (California Digital Library) (submittedVersion)
- PMC
- Funders
- PRESTO from the Japan Science and Technology (JST) Agency
- Drug Discovery and Informatics
- Japan Society for the Promotion of Science (JSPS)
- Core Research for Evolutional Science and Technology (CREST)
- Japan Science and Technology Agency (JST)
- NIH (5DP1-MH100706)
- Keck
- McKnight
- Poitras
- Merkin
- Vallee
- Damon Runyon
- Searle Scholars
- Klingenstein
- Simons Foundations
- Bob Metcalfe
- Jane Pauley
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Enzyme Structure and Function
- Keywords
- CRISPR/Cas12a, guide RNA, target DNA, RNA-guided DNA cleavage, protospacer adjacent motif, genome editing, crystal structure
- MeSH terms
- Amino Acid Sequence, Bacteria, DNA, Bacterial, Endonucleases, Models, Molecular, Molecular Sequence Data, RNA, Bacterial, Streptococcus pyogenes, Sequence Alignment, Protein Structure, Tertiary, Crystallography, X-Ray, RNA, Small Untranslated, CRISPR-Associated Proteins
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