Characterization and applications of Type I CRISPR-Cas systems

Hidalgo-Cantabrana, Claudio; Barrangou, Rodolphe

doi:10.1042/bst20190119

Title: Characterization and applications of Type I CRISPR-Cas systems

Journal Article · 09 January 2020 · Biochemical Society Transactions

DOI: https://doi.org/10.1042/bst20190119 · OSTI ID:1889422

Hidalgo-Cantabrana, Claudio ^[1];

^[1]

North Carolina State Univ., Raleigh, NC (United States)

CRISPR-Cas constitutes the adaptive immune system of bacteria and archaea. This RNA-mediated sequence-specific recognition and targeting machinery has been used broadly for diverse applications in a wide range of organisms across the tree of life. The compact class 2 systems, that hinge on a single Cas effector nuclease have been harnessed for genome editing, transcriptional regulation, detection, imaging and other applications, in different research areas. However, most of the CRISPR-Cas systems belong to class 1, and the molecular machinery of the most widespread and diverse Type I systems afford tremendous opportunities for a broad range of applications. These highly abundant systems rely on a multi-protein effector complex, the CRISPR associated complex for antiviral defense (Cascade), which drives DNA targeting and cleavage. The complexity of these systems has somewhat hindered their widespread usage, but the pool of thousands of diverse Type I CRISPR-Cas systems opens new avenues for CRISPR-based applications in bacteria, archaea and eukaryotes. Here, we describe the features and mechanism of action of Type I CRISPR-Cas systems, illustrate how endogenous systems can be reprogrammed to target the host genome and perform genome editing and transcriptional regulation by co-delivering a minimal CRISPR array together with a repair template. Moreover, we discuss how these systems can also be used in eukaryotes. Finally, this review provides a framework for expanding the CRISPR toolbox, and repurposing the most abundant CRISPR-Cas systems for a wide range of applications.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); North Carolina State Univ., Raleigh, NC (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1889422

Journal Information:: Biochemical Society Transactions, Journal Name: Biochemical Society Transactions Journal Issue: 1 Vol. 48; ISSN 0300-5127

Publisher:: Portland PressCopyright Statement

Country of Publication:: United States

Language:: English

References (58)

Molecular mechanisms of CRISPR-mediated microbial immunity Gasiunas, Giedrius; Sinkunas, Tomas; Siksnys, Virginijus Cellular and Molecular Life Sciences, Vol. 71, Issue 3 https://doi.org/10.1007/s00018-013-1438-6	journal	August 2013
Intervening Sequences of Regularly Spaced Prokaryotic Repeats Derive from Foreign Genetic Elements Mojica, Francisco J. M.; D�ez-Villase�or, Chc)sar; Garc�a-Mart�nez, Jes�s Journal of Molecular Evolution, Vol. 60, Issue 2 https://doi.org/10.1007/s00239-004-0046-3	journal	February 2005
Repurposing CRISPR as an RNA-Guided Platform for Sequence-Specific Control of Gene Expression Qi, Lei S.; Larson, Matthew H.; Gilbert, Luke A. Cell, Vol. 152, Issue 5, p. 1173-1183 https://doi.org/10.1016/j.cell.2013.02.022	journal	February 2013
SnapShot: Class 2 CRISPR-Cas Systems Makarova, Kira S.; Zhang, Feng; Koonin, Eugene V. Cell, Vol. 168, Issue 1-2 https://doi.org/10.1016/j.cell.2016.12.038	journal	January 2017
SnapShot: Class 1 CRISPR-Cas Systems Makarova, Kira S.; Zhang, Feng; Koonin, Eugene V. Cell, Vol. 168, Issue 5 https://doi.org/10.1016/j.cell.2017.02.018	journal	February 2017
Structure Basis for Directional R-loop Formation and Substrate Handover Mechanisms in Type I CRISPR-Cas System Xiao, Yibei; Luo, Min; Hayes, Robert P. Cell, Vol. 170, Issue 1 https://doi.org/10.1016/j.cell.2017.06.012	journal	June 2017
Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression Qi, Lei S.; Larson, Matthew H.; Gilbert, Luke A. Cell, Vol. 184, Issue 3 https://doi.org/10.1016/j.cell.2021.01.019	journal	February 2021
Harnessing the native type I-B CRISPR-Cas for genome editing in a polyploid archaeon Cheng, Feiyue; Gong, Luyao; Zhao, Dahe Journal of Genetics and Genomics, Vol. 44, Issue 11 https://doi.org/10.1016/j.jgg.2017.09.010	journal	November 2017
Characterization and Repurposing of Type I and Type II CRISPR–Cas Systems in Bacteria Hidalgo-Cantabrana, Claudio; Goh, Yong Jun; Barrangou, Rodolphe Journal of Molecular Biology, Vol. 431, Issue 1 https://doi.org/10.1016/j.jmb.2018.09.013	journal	January 2019
Diversity, classification and evolution of CRISPR-Cas systems Koonin, Eugene V.; Makarova, Kira S.; Zhang, Feng Current Opinion in Microbiology, Vol. 37 https://doi.org/10.1016/j.mib.2017.05.008	journal	June 2017
CRISPR Immunity Relies on the Consecutive Binding and Degradation of Negatively Supercoiled Invader DNA by Cascade and Cas3 Westra, Edze R.; van Erp, Paul B. G.; Künne, Tim Molecular Cell, Vol. 46, Issue 5 https://doi.org/10.1016/j.molcel.2012.03.018	journal	June 2012
Identifying and Visualizing Functional PAM Diversity across CRISPR-Cas Systems Leenay, Ryan T.; Maksimchuk, Kenneth R.; Slotkowski, Rebecca A. Molecular Cell, Vol. 62, Issue 1 https://doi.org/10.1016/j.molcel.2016.02.031	journal	April 2016
DNA Targeting by a Minimal CRISPR RNA-Guided Cascade Hochstrasser, Megan L.; Taylor, David W.; Kornfeld, Jack E. Molecular Cell, Vol. 63, Issue 5 https://doi.org/10.1016/j.molcel.2016.07.027	journal	September 2016
Expanding the CRISPR Toolbox: Targeting RNA with Cas13b Barrangou, Rodolphe; Gersbach, Charles A. Molecular Cell, Vol. 65, Issue 4 https://doi.org/10.1016/j.molcel.2017.02.002	journal	February 2017
Structural Variation of Type I-F CRISPR RNA Guided DNA Surveillance Pausch, Patrick; Müller-Esparza, Hanna; Gleditzsch, Daniel Molecular Cell, Vol. 67, Issue 4 https://doi.org/10.1016/j.molcel.2017.06.036	journal	August 2017
Repetitive DNA Reeling by the Cascade-Cas3 Complex in Nucleotide Unwinding Steps Loeff, Luuk; Brouns, Stan J. J.; Joo, Chirlmin Molecular Cell, Vol. 70, Issue 3 https://doi.org/10.1016/j.molcel.2018.03.031	journal	May 2018
Introducing a Spectrum of Long-Range Genomic Deletions in Human Embryonic Stem Cells Using Type I CRISPR-Cas Dolan, Adam E.; Hou, Zhonggang; Xiao, Yibei Molecular Cell, Vol. 74, Issue 5 https://doi.org/10.1016/j.molcel.2019.03.014	journal	June 2019
Interaction of the Cas6 Riboendonuclease with CRISPR RNAs: Recognition and Cleavage Wang, Ruiying; Preamplume, Gan; Terns, Michael P. Structure, Vol. 19, Issue 2 https://doi.org/10.1016/j.str.2010.11.014	journal	February 2011
Structural Principles of CRISPR RNA Processing Li, Hong Structure, Vol. 23, Issue 1 https://doi.org/10.1016/j.str.2014.10.006	journal	January 2015
Advances in Industrial Biotechnology Using CRISPR-Cas Systems Donohoue, Paul D.; Barrangou, Rodolphe; May, Andrew P. Trends in Biotechnology, Vol. 36, Issue 2 https://doi.org/10.1016/j.tibtech.2017.07.007	journal	February 2018
Exploiting endogenous CRISPR-Cas system for multiplex genome editing in Clostridium tyrobutyricum and engineer the strain for high-level butanol production Zhang, Jie; Zong, Wenming; Hong, Wei Metabolic Engineering, Vol. 47 https://doi.org/10.1016/j.ymben.2018.03.007	journal	May 2018
Cas3 is a single-stranded DNA nuclease and ATP-dependent helicase in the CRISPR/Cas immune system: Cas3 nuclease/helicase Sinkunas, Tomas; Gasiunas, Giedrius; Fremaux, Christophe The EMBO Journal, Vol. 30, Issue 7 https://doi.org/10.1038/emboj.2011.41	journal	February 2011
In vitro reconstitution of Cascade-mediated CRISPR immunity in Streptococcus thermophilus Sinkunas, Tomas; Gasiunas, Giedrius; Waghmare, Sakharam P. The EMBO Journal, Vol. 32, Issue 3 https://doi.org/10.1038/emboj.2012.352	journal	January 2013
Self versus non-self discrimination during CRISPR RNA-directed immunity Marraffini, Luciano A.; Sontheimer, Erik J. Nature, Vol. 463, Issue 7280 https://doi.org/10.1038/nature08703	journal	January 2010
RNA-guided editing of bacterial genomes using CRISPR-Cas systems Jiang, Wenyan; Bikard, David; Cox, David Nature Biotechnology, Vol. 31, Issue 3, p. 233-239 https://doi.org/10.1038/nbt.2508	journal	January 2013
Sequence-specific antimicrobials using efficiently delivered RNA-guided nucleases Citorik, Robert J.; Mimee, Mark; Lu, Timothy K. Nature Biotechnology, Vol. 32, Issue 11 https://doi.org/10.1038/nbt.3011	journal	September 2014
Applications of CRISPR technologies in research and beyond Barrangou, Rodolphe; Doudna, Jennifer A. Nature Biotechnology, Vol. 34, Issue 9 https://doi.org/10.1038/nbt.3659	journal	September 2016
CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea Marraffini, Luciano A.; Sontheimer, Erik J. Nature Reviews Genetics, Vol. 11, Issue 3 https://doi.org/10.1038/nrg2749	journal	February 2010
Structural basis for CRISPR RNA-guided DNA recognition by Cascade Jore, Matthijs M.; Lundgren, Magnus; van Duijn, Esther Nature Structural & Molecular Biology, Vol. 18, Issue 5 https://doi.org/10.1038/nsmb.2019	journal	April 2011
Structures of CRISPR Cas3 offer mechanistic insights into Cascade-activated DNA unwinding and degradation Huo, Yanwu; Nam, Ki Hyun; Ding, Fang Nature Structural & Molecular Biology, Vol. 21, Issue 9 https://doi.org/10.1038/nsmb.2875	journal	August 2014
CRISPR-Cas3 induces broad and unidirectional genome editing in human cells Morisaka, Hiroyuki; Yoshimi, Kazuto; Okuzaki, Yuya Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13226-x	journal	December 2019
Targeted transcriptional modulation with type I CRISPR–Cas systems in human cells Pickar-Oliver, Adrian; Black, Joshua B.; Lewis, Mae M. Nature Biotechnology, Vol. 37, Issue 12 https://doi.org/10.1038/s41587-019-0235-7	journal	September 2019
The repurposing of type I-E CRISPR-Cascade for gene activation in plants Young, Joshua K.; Gasior, Stephen L.; Jones, Spencer Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0637-6	journal	October 2019
Harnessing heterologous and endogenous CRISPR-Cas machineries for efficient markerless genome editing in Clostridium Pyne, Michael E.; Bruder, Mark R.; Moo-Young, Murray Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep25666	journal	May 2016
Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence Semenova, E.; Jore, M. M.; Datsenko, K. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue 25, p. 10098-10103 https://doi.org/10.1073/pnas.1104144108	journal	June 2011
Spacer capture and integration by a type I-F Cas1–Cas2-3 CRISPR adaptation complex Fagerlund, Robert D.; Wilkinson, Max E.; Klykov, Oleg Proceedings of the National Academy of Sciences https://doi.org/10.1073/pnas.1618421114	journal	June 2017
Genome editing using the endogenous type I CRISPR-Cas system in Lactobacillus crispatus Hidalgo-Cantabrana, Claudio; Goh, Yong Jun; Pan, Meichen Proceedings of the National Academy of Sciences, Vol. 116, Issue 32 https://doi.org/10.1073/pnas.1905421116	journal	July 2019
In Vitro Reconstitution of an Escherichia coli RNA-guided Immune System Reveals Unidirectional, ATP-dependent Degradation of DNA Target Mulepati, Sabin; Bailey, Scott Journal of Biological Chemistry, Vol. 288, Issue 31 https://doi.org/10.1074/jbc.M113.472233	journal	June 2013
A Ruler Protein in a Complex for Antiviral Defense Determines the Length of Small Interfering CRISPR RNAs Hatoum-Aslan, Asma; Samai, Poulami; Maniv, Inbal Journal of Biological Chemistry, Vol. 288, Issue 39 https://doi.org/10.1074/jbc.M113.499244	journal	August 2013
Gene Repression in Haloarchaea Using the CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats)-Cas I-B System Stachler, Aris-Edda; Marchfelder, Anita Journal of Biological Chemistry, Vol. 291, Issue 29 https://doi.org/10.1074/jbc.M116.724062	journal	May 2016
CRISPRdisco: An Automated Pipeline for the Discovery and Analysis of CRISPR-Cas Systems Crawley, Alexandra B.; Henriksen, James R.; Barrangou, Rodolphe The CRISPR Journal, Vol. 1, Issue 2 https://doi.org/10.1089/crispr.2017.0022	journal	April 2018
Classification and Nomenclature of CRISPR-Cas Systems: Where from Here? Makarova, Kira S.; Wolf, Yuri I.; Koonin, Eugene V. The CRISPR Journal, Vol. 1, Issue 5 https://doi.org/10.1089/crispr.2018.0033	journal	October 2018
Repurposing endogenous type I CRISPR-Cas systems for programmable gene repression Luo, Michelle L.; Mullis, Adam S.; Leenay, Ryan T. Nucleic Acids Research, Vol. 43, Issue 1 https://doi.org/10.1093/nar/gku971	journal	October 2014
Harnessing Type I and Type III CRISPR-Cas systems for genome editing Li, Yingjun; Pan, Saifu; Zhang, Yan Nucleic Acids Research, Vol. 44, Issue 4 https://doi.org/10.1093/nar/gkv1044	journal	October 2015
Modulating the Cascade architecture of a minimal Type I-F CRISPR-Cas system Gleditzsch, Daniel; Müller-Esparza, Hanna; Pausch, Patrick Nucleic Acids Research, Vol. 44, Issue 12 https://doi.org/10.1093/nar/gkw469	journal	May 2016
Altered stoichiometry Escherichia coli Cascade complexes with shortened CRISPR RNA spacers are capable of interference and primed adaptation Kuznedelov, Konstantin; Mekler, Vladimir; Lemak, Sofia Nucleic Acids Research, Vol. 44, Issue 22 https://doi.org/10.1093/nar/gkw914	journal	October 2016
Short motif sequences determine the targets of the prokaryotic CRISPR defence system Mojica, F. J. M.; Díez-Villaseñor, C.; García-Martínez, J. Microbiology, Vol. 155, Issue 3, p. 733-740 https://doi.org/10.1099/mic.0.023960-0	journal	March 2009
Diversity of CRISPR loci in Escherichia coli Díez-Villaseñor, C.; Almendros, C.; García-Martínez, J. Microbiology, Vol. 156, Issue 5 https://doi.org/10.1099/mic.0.036046-0	journal	May 2010
CRISPR Provides Acquired Resistance Against Viruses in Prokaryotes Barrangou, R.; Fremaux, C.; Deveau, H. Science, Vol. 315, Issue 5819 https://doi.org/10.1126/science.1138140	journal	March 2007
Small CRISPR RNAs Guide Antiviral Defense in Prokaryotes Brouns, S. J. J.; Jore, M. M.; Lundgren, M. Science, Vol. 321, Issue 5891, p. 960-964 https://doi.org/10.1126/science.1159689	journal	August 2008
CRISPR-Cas guides the future of genetic engineering Knott, Gavin J.; Doudna, Jennifer A. Science, Vol. 361, Issue 6405 https://doi.org/10.1126/science.aat5011	journal	August 2018
Programmed DNA destruction by miniature CRISPR-Cas14 enzymes Harrington, Lucas B.; Burstein, David; Chen, Janice S. Science, Vol. 362, Issue 6416 https://doi.org/10.1126/science.aav4294	journal	October 2018
Phage Response to CRISPR-Encoded Resistance in Streptococcus thermophilus Deveau, H.; Barrangou, R.; Garneau, J. E. Journal of Bacteriology, Vol. 190, Issue 4 https://doi.org/10.1128/JB.01412-07	journal	December 2007
Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. Ishino, Y.; Shinagawa, H.; Makino, K. Journal of Bacteriology, Vol. 169, Issue 12 https://doi.org/10.1128/jb.169.12.5429-5433.1987	journal	December 1987
Programmable Removal of Bacterial Strains by Use of Genome-Targeting CRISPR-Cas Systems Gomaa, Ahmed A.; Klumpe, Heidi E.; Luo, Michelle L. mBio, Vol. 5, Issue 1 https://doi.org/10.1128/mBio.00928-13	journal	January 2014
Easy regulation of metabolic flux in Escherichia coli using an endogenous type I-E CRISPR-Cas system Chang, Yizhao; Su, Tianyuan; Qi, Qingsheng Microbial Cell Factories, Vol. 15, Issue 1 https://doi.org/10.1186/s12934-016-0594-4	journal	November 2016
Characterization and Exploitation of CRISPR Loci in Bifidobacterium longum Hidalgo-Cantabrana, Claudio; Crawley, Alexandra B.; Sanchez, Borja Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01851	journal	September 2017
Efficient engineering of a bacteriophage genome using the type I-E CRISPR-Cas system Kiro, Ruth; Shitrit, Dror; Qimron, Udi RNA Biology, Vol. 11, Issue 1 https://doi.org/10.4161/rna.27766	journal	January 2014

Similar Records

Structural organization of a Type III-A CRISPR effector subcomplex determined by X-ray crystallography and cryo-EM

Journal Article · 2019 · Nucleic Acids Research · OSTI ID:1544886

Dorsey, Bryan W.; Huang, Lei; Mondragón, Alfonso

Structural basis for AcrVA4 inhibition of specific CRISPR-Cas12a

Journal Article · 2019 · eLife · OSTI ID:1560609

Knott, Gavin J.; Cress, Brady F.; Liu, Jun-Jie; +11 more

System-level perturbations of cell metabolism using CRISPR/Cas9

Journal Article · 2017 · Current Opinion in Biotechnology · OSTI ID:1393248

Jakočiūnas, Tadas; Jensen, Michael K.; Keasling, Jay D.

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
CRISPR
Cas
Gene expression & regulation
Genome editing
Genomics
Microbiology
Type I

Title: Characterization and applications of Type I CRISPR-Cas systems

Citation Formats

References (58)

Similar Records

Related Subjects