Cas9 gRNA engineering for genome editing, activation and repression

Kiani, Samira; Chavez, Alejandro; Tuttle, Marcelle; Hall, Richard N.; Chari, Raj; Ter-Ovanesyan, Dmitry; Qian, Jason; Pruitt, Benjamin W.; Beal, Jacob; Vora, Suhani; Buchthal, Joanna; Kowal, Emma J. K.; Ebrahimkhani, Mohammad R.; Collins, James J.; Weiss, Ron; Church, George

doi:10.1038/nmeth.3580

Title: Cas9 gRNA engineering for genome editing, activation and repression

Abstract

Here we demonstrate that by altering the length of Cas9-associated guide RNA(gRNA) we were able to control Cas9 nuclease activity and simultaneously perform genome editing and transcriptional regulation with a single Cas9 protein. We exploited these principles to engineer mammalian synthetic circuits with combined transcriptional regulation and kill functions governed by a single multifunctional Cas9 protein.

Authors:

Kiani, Samira ^[1]; Chavez, Alejandro ^[2]; Tuttle, Marcelle ^[3]; Hall, Richard N. ^[1]; Chari, Raj ^[4]; Ter-Ovanesyan, Dmitry ^[5]; Qian, Jason ^[5]; Pruitt, Benjamin W. ^[3];

^[6];

^[7]; Buchthal, Joanna ^[3]; Kowal, Emma J. K. ^[3]; Ebrahimkhani, Mohammad R. ^[1]; Collins, James J. ^[8]; Weiss, Ron ^[1]; Church, George ^[5]

Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Harvard Univ., Cambridge, MA (United States); Massachusetts Hospital, Boston, MA (United States); Harvard Medical School, Boston, MA (United States)
Harvard Univ., Cambridge, MA (United States)
Harvard Medical School, Boston, MA (United States)
Harvard Univ., Cambridge, MA (United States); Harvard Medical School, Boston, MA (United States)
Raytheon BBN Technologies, Cambridge, MA (United States)
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Harvard Univ., Cambridge, MA (United States); Harvard Medical School, Boston, MA (United States)
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Harvard Univ., Cambridge, MA (United States); Broad Institute of MIT and Harvard, Cambridge, MA (United States); Harvard-MIT Program in Health Sciences and Technology, Cambridge, MA (United States)

Publication Date:: Mon Sep 07 00:00:00 EDT 2015

Research Org.:: Harvard Univ., Cambridge, MA (United States)

Sponsoring Org.:: USDOE

OSTI Identifier:: 1347131

Grant/Contract Number:: FG02-02ER63445

Resource Type:: Accepted Manuscript

Journal Name:: Nature Methods

Additional Journal Information:: Journal Volume: 12; Journal Issue: 11; Journal ID: ISSN 1548-7091

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Kiani, Samira, Chavez, Alejandro, Tuttle, Marcelle, Hall, Richard N., Chari, Raj, Ter-Ovanesyan, Dmitry, Qian, Jason, Pruitt, Benjamin W., Beal, Jacob, Vora, Suhani, Buchthal, Joanna, Kowal, Emma J. K., Ebrahimkhani, Mohammad R., Collins, James J., Weiss, Ron, and Church, George. Cas9 gRNA engineering for genome editing, activation and repression.  United States: N. p., 2015. 
Web.  doi:10.1038/nmeth.3580.

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                    Kiani, Samira, Chavez, Alejandro, Tuttle, Marcelle, Hall, Richard N., Chari, Raj, Ter-Ovanesyan, Dmitry, Qian, Jason, Pruitt, Benjamin W., Beal, Jacob, Vora, Suhani, Buchthal, Joanna, Kowal, Emma J. K., Ebrahimkhani, Mohammad R., Collins, James J., Weiss, Ron, & Church, George. Cas9 gRNA engineering for genome editing, activation and repression.  United States.  https://doi.org/10.1038/nmeth.3580

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                    Kiani, Samira, Chavez, Alejandro, Tuttle, Marcelle, Hall, Richard N., Chari, Raj, Ter-Ovanesyan, Dmitry, Qian, Jason, Pruitt, Benjamin W., Beal, Jacob, Vora, Suhani, Buchthal, Joanna, Kowal, Emma J. K., Ebrahimkhani, Mohammad R., Collins, James J., Weiss, Ron, and Church, George. Mon .  
"Cas9 gRNA engineering for genome editing, activation and repression".  United States.  https://doi.org/10.1038/nmeth.3580.  https://www.osti.gov/servlets/purl/1347131.

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@article{osti_1347131,

  title        = {Cas9 gRNA engineering for genome editing, activation and repression},

  author       = {Kiani, Samira and Chavez, Alejandro and Tuttle, Marcelle and Hall, Richard N. and Chari, Raj and Ter-Ovanesyan, Dmitry and Qian, Jason and Pruitt, Benjamin W. and Beal, Jacob and Vora, Suhani and Buchthal, Joanna and Kowal, Emma J. K. and Ebrahimkhani, Mohammad R. and Collins, James J. and Weiss, Ron and Church, George},

  abstractNote = {Here we demonstrate that by altering the length of Cas9-associated guide RNA(gRNA) we were able to control Cas9 nuclease activity and simultaneously perform genome editing and transcriptional regulation with a single Cas9 protein. We exploited these principles to engineer mammalian synthetic circuits with combined transcriptional regulation and kill functions governed by a single multifunctional Cas9 protein.},

  doi          = {10.1038/nmeth.3580},

  journal      = {Nature Methods},

  number       = 11,

  volume       = 12,

  place        = {United States},

  year         = {Mon Sep 07 00:00:00 EDT 2015},

  month        = {Mon Sep 07 00:00:00 EDT 2015}

}

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DOI: 10.3929/ethz-b-000364039

Rewiring of endogenous signaling pathways to genomic targets for therapeutic cell reprogramming
text, January 2020

Krawczyk, Krzysztof; Scheller, Leo; Kim, Hyojin
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A multiplex guide RNA expression system and its efficacy for plant genome engineering
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A multiplex guide RNA expression system and its efficacy for plant genome engineering
posted_content, March 2020

Oh, Youngbin; Lee, Bora; Kim, Hyeonjin
DOI: 10.21203/rs.2.21279/v4

Suppression of unwanted CRISPR-Cas9 editing by co-administration of catalytically inactivating truncated guide RNAs
text, January 2020

Rose, John C.; Popp, Nicholas A.; Richardson, Christopher D.
ETH Zurich
DOI: 10.3929/ethz-b-000419359

Multistable and dynamic CRISPRi-based synthetic circuits
text, January 2020

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DOI: 10.3929/ethz-b-000419893

Crossing enhanced and high fidelity SpCas9 nucleases to optimize specificity and cleavage
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A multiplex guide RNA expression system and its efficacy for plant genome engineering
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Oh, Youngbin; Lee, Bora; Kim, Hyeonjin
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The Chromatin Structure Differentially Impacts High-Specificity CRISPR-Cas9 Nuclease Strategies
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Chen, Xiaoyu; Liu, Jin; Janssen, Josephine M.
Molecular Therapy - Nucleic Acids, Vol. 8
DOI: 10.1016/j.omtn.2017.08.005

Integration and exchange of split dCas9 domains for transcriptional controls in mammalian cells
journal, October 2016

Ma, Dacheng; Peng, Shuguang; Xie, Zhen
Nature Communications, Vol. 7, Issue 1
DOI: 10.1038/ncomms13056

Hit and go CAS9 delivered through a lentiviral based self-limiting circuit
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Petris, Gianluca; Casini, Antonio; Montagna, Claudia
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DOI: 10.1038/ncomms15334

Optimizing genome editing strategy by primer-extension-mediated sequencing
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DOI: 10.1038/s41421-019-0088-8

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DOI: 10.1038/s41467-017-01695-x

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Kocak, D. Dewran; Josephs, Eric A.; Bhandarkar, Vidit
Nature Biotechnology, Vol. 37, Issue 6
DOI: 10.1038/s41587-019-0095-1

Towards personalised allele-specific CRISPR gene editing to treat autosomal dominant disorders
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Christie, Kathleen A.; Courtney, David G.; DeDionisio, Larry A.
Scientific Reports, Vol. 7, Issue 1
DOI: 10.1038/s41598-017-16279-4

Transcriptional control by enhancers and enhancer RNAs
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Lewis, Michael W.; Li, Shen; Franco, Hector L.
Transcription, Vol. 10, Issue 4-5
DOI: 10.1080/21541264.2019.1695492

Design principles for nuclease-deficient CRISPR-based transcriptional regulators
journal, April 2018

Jensen, Michael K.
FEMS Yeast Research, Vol. 18, Issue 4
DOI: 10.1093/femsyr/foy039

Systematical study of the mechanistic factors regulating genome dynamics in vivo by CRISPRsie
journal, July 2019

Han, Deqiang; Hong, Yu; Mai, Xueying
Journal of Molecular Cell Biology, Vol. 11, Issue 11
DOI: 10.1093/jmcb/mjz074

Guide RNA engineering for versatile Cas9 functionality
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Nowak, Chance M.; Lawson, Seth; Zerez, Megan
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DOI: 10.1093/nar/gkw908

Creation of versatile cloning platforms for transgene expression and dCas9-based epigenome editing
journal, December 2018

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DOI: 10.1093/nar/gky1286

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Zhan, Hengji; Zhou, Qun; Gao, Qunjun
Genome Biology, Vol. 20, Issue 1
DOI: 10.1186/s13059-019-1712-5

Modulating chromatin accessibility by transactivation and targeting proximal dsgRNAs enhances Cas9 editing efficiency in vivo
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DOI: 10.1186/s13059-019-1762-8

Precision Modulation of Neurodegenerative Disease-Related Gene Expression in Human iPSC-Derived Neurons
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Andrew, Wood, Matthew John; Mahalia, Heman-Ackah, Sabrina; Roger, Bassett, Andrew
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DOI: 10.17615/491c-tm73

Transgenic Mouse Models in Cancer Research
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Modeling Neuropsychiatric and Neurodegenerative Diseases With Induced Pluripotent Stem Cells
journal, April 2018

LaMarca, Elizabeth A.; Powell, Samuel K.; Akbarian, Schahram
Frontiers in Pediatrics, Vol. 6
DOI: 10.3389/fped.2018.00082

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Title: Cas9 gRNA engineering for genome editing, activation and repression

Abstract

Citation Formats

Development and Applications of CRISPR-Cas9 for Genome Engineering journal, June 2014

CRISPR-Cas systems for editing, regulating and targeting genomes journal, March 2014

Repurposing CRISPR as an RNA-Guided Platform for Sequence-Specific Control of Gene Expression journal, February 2013

Cas9 as a versatile tool for engineering biology journal, September 2013

Improving CRISPR-Cas nuclease specificity using truncated guide RNAs journal, January 2014

RNA-guided editing of bacterial genomes using CRISPR-Cas systems journal, January 2013

Highly efficient Cas9-mediated transcriptional programming journal, March 2015

Orthogonal Cas9 proteins for RNA-guided gene regulation and editing journal, September 2013

CRISPR transcriptional repression devices and layered circuits in mammalian cells journal, May 2014

Multiplexed and Programmable Regulation of Gene Networks with an Integrated RNA and CRISPR/Cas Toolkit in Human Cells journal, May 2014

Modular construction of mammalian gene circuits using TALE transcriptional repressors journal, February 2015

Accurate Predictions of Genetic Circuit Behavior from Part Characterization and Modular Composition journal, November 2014

Inducible in vivo genome editing with CRISPR-Cas9 journal, February 2015

CRISPR-Cas9 Knockin Mice for Genome Editing and Cancer Modeling journal, October 2014

RNA-guided gene activation by CRISPR-Cas9–based transcription factors journal, July 2013

CRISPR RNA–guided activation of endogenous human genes journal, July 2013

Dynamic Imaging of Genomic Loci in Living Human Cells by an Optimized CRISPR/Cas System journal, December 2013

FLASH: fast length adjustment of short reads to improve genome assemblies journal, September 2011

Fast and accurate short read alignment with Burrows-Wheeler transform journal, May 2009

The Sequence Alignment/Map format and SAMtools journal, June 2009

RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome journal, August 2011

voom: precision weights unlock linear model analysis tools for RNA-seq read counts journal, January 2014

Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments journal, January 2004

NIST/ISAC standardization study: Variability in assignment of intensity values to fluorescence standard beads and in cross calibration of standard beads to hard dyed beads journal, June 2012

Bridging the Gap: A Roadmap to Breaking the Biological Design Barrier journal, January 2015

Dynamic Imaging of Genomic Loci in Living Human Cells by an Optimized CRISPR/Cas System journal, January 2014

OmicLoupe: facilitating biological discovery by interactive exploration of multiple omic datasets and statistical comparisons journal, March 2021

Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression journal, February 2021

CRISPR Technology for Breast Cancer: Diagnostics, Modeling, and Therapy journal, August 2018

Combining orthogonal CRISPR and CRISPRi systems for genome engineering and metabolic pathway modulation in Escherichia coli journal, February 2019

Attenuation of Inherited and Acquired Retinal Degeneration Progression with Gene-based Techniques journal, December 2018

Orthogonal gene knockout and activation with a catalytically active Cas9 nuclease journal, October 2015

Multiplexed labeling of genomic loci with dCas9 and engineered sgRNAs using CRISPRainbow journal, April 2016

Partial DNA-guided Cas9 enables genome editing with reduced off-target activity journal, January 2018

Hit and go CAS9 delivered through a lentiviral based self-limiting circuit journal, May 2017

Editing the epigenome: technologies for programmable transcription and epigenetic modulation journal, January 2016

A multifunctional AAV–CRISPR–Cas9 and its host response journal, September 2016

Complex transcriptional modulation with orthogonal and inducible dCas9 regulators journal, October 2016

Rapidly inducible Cas9 and DSB-ddPCR to probe editing kinetics journal, July 2017

Genome-scale CRISPR-Cas9 knockout and transcriptional activation screening journal, March 2017

Defining and improving the genome-wide specificities of CRISPR–Cas9 nucleases journal, April 2016

Programmable DNA repair with CRISPRa/i enhanced homology-directed repair efficiency with a single Cas9 journal, July 2018

Combinatorial metabolic engineering using an orthogonal tri-functional CRISPR system journal, November 2017

Site-specific manipulation of Arabidopsis loci using CRISPR-Cas9 SunTag systems journal, February 2019

Multi-functional genome-wide CRISPR system for high throughput genotype–phenotype mapping journal, December 2019

Rewiring of endogenous signaling pathways to genomic targets for therapeutic cell reprogramming journal, January 2020

The emerging and uncultivated potential of CRISPR technology in plant science journal, July 2019

Increasing the specificity of CRISPR systems with engineered RNA secondary structures journal, April 2019

Multiplexed orthogonal genome editing and transcriptional activation by Cas12a journal, December 2018

Multiplexed genome engineering by Cas12a and CRISPR arrays encoded on single transcripts journal, August 2019

CRISPR RNA-guided autonomous delivery of Cas9 journal, December 2018

Precision Modulation of Neurodegenerative Disease-Related Gene Expression in Human iPSC-Derived Neurons journal, June 2016

Graphene oxide-mediated Cas9/sgRNA delivery for efficient genome editing journal, January 2018

A CRISPR/Cas9-based central processing unit to program complex logic computation in human cells journal, March 2019

Transcriptional control by enhancers and enhancer RNAs journal, October 2019

CRISPR-Cas9 nuclear dynamics and target recognition in living cells journal, August 2016

The physicist’s guide to one of biotechnology’s hottest new topics: CRISPR-Cas journal, April 2018

Recent advances in developing and applying biosensors for synthetic biology journal, October 2019

Systematical study of the mechanistic factors regulating genome dynamics in vivo by CRISPRsie journal, July 2019

Creation of versatile cloning platforms for transgene expression and dCas9-based epigenome editing journal, December 2018

CRISPR-assisted multi-dimensional regulation for fine-tuning gene expression in Bacillus subtilis journal, February 2019

PERSIST: A programmable RNA regulation platform using CRISPR endoRNases preprint, December 2019

CRISPR Tools for Systematic Studies of RNA Regulation journal, August 2019

A Model for Resource Competition in CRISPR-Mediated Gene Repression conference, December 2018

A revolutionary tool: CRISPR technology plays an important role in construction of intelligentized gene circuits journal, November 2018

Potential pitfalls of CRISPR/Cas9-mediated genome editing journal, November 2015

Next stop for the CRISPR revolution: RNA-guided epigenetic regulators journal, July 2016

Optimized paired-sgRNA/Cas9 cloning and expression cassette triggers high-efficiency multiplex genome editing in kiwifruit journal, February 2018

Disabling Cas9 by an anti-CRISPR DNA mimic journal, July 2017

Programming gene and engineered-cell therapies with synthetic biology journal, February 2018

C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector journal, June 2016

CRISPR-mediated activation of a promoter or enhancer rescues obesity caused by haploinsufficiency journal, December 2018

A multiplex guide RNA expression system and its efficacy for plant genome engineering journal, March 2020

Crossing enhanced and high fidelity SpCas9 nucleases to optimize specificity and cleavage journal, October 2017

Multiplexed promoterless gene expression with CRISPReader journal, June 2019

Modulating chromatin accessibility by transactivation and targeting proximal dsgRNAs enhances Cas9 editing efficiency in vivo journal, July 2019

SWISS: multiplexed orthogonal genome editing in plants with a Cas9 nickase and engineered CRISPR RNA scaffolds journal, June 2020

Development and Applications of CRISPR-Cas9 for Genome Engineering
journal, June 2014

CRISPR-Cas systems for editing, regulating and targeting genomes
journal, March 2014

Repurposing CRISPR as an RNA-Guided Platform for Sequence-Specific Control of Gene Expression
journal, February 2013

Cas9 as a versatile tool for engineering biology
journal, September 2013

Improving CRISPR-Cas nuclease specificity using truncated guide RNAs
journal, January 2014

RNA-guided editing of bacterial genomes using CRISPR-Cas systems
journal, January 2013

Highly efficient Cas9-mediated transcriptional programming
journal, March 2015

Orthogonal Cas9 proteins for RNA-guided gene regulation and editing
journal, September 2013

CRISPR transcriptional repression devices and layered circuits in mammalian cells
journal, May 2014

Multiplexed and Programmable Regulation of Gene Networks with an Integrated RNA and CRISPR/Cas Toolkit in Human Cells
journal, May 2014

Modular construction of mammalian gene circuits using TALE transcriptional repressors
journal, February 2015

Accurate Predictions of Genetic Circuit Behavior from Part Characterization and Modular Composition
journal, November 2014

Inducible in vivo genome editing with CRISPR-Cas9
journal, February 2015

CRISPR-Cas9 Knockin Mice for Genome Editing and Cancer Modeling
journal, October 2014

RNA-guided gene activation by CRISPR-Cas9–based transcription factors
journal, July 2013

CRISPR RNA–guided activation of endogenous human genes
journal, July 2013

Dynamic Imaging of Genomic Loci in Living Human Cells by an Optimized CRISPR/Cas System
journal, December 2013

FLASH: fast length adjustment of short reads to improve genome assemblies
journal, September 2011

Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009

The Sequence Alignment/Map format and SAMtools
journal, June 2009

RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome
journal, August 2011

voom: precision weights unlock linear model analysis tools for RNA-seq read counts
journal, January 2014

Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments
journal, January 2004

NIST/ISAC standardization study: Variability in assignment of intensity values to fluorescence standard beads and in cross calibration of standard beads to hard dyed beads
journal, June 2012

Bridging the Gap: A Roadmap to Breaking the Biological Design Barrier
journal, January 2015

Dynamic Imaging of Genomic Loci in Living Human Cells by an Optimized CRISPR/Cas System
journal, January 2014

OmicLoupe: facilitating biological discovery by interactive exploration of multiple omic datasets and statistical comparisons
journal, March 2021

Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression
journal, February 2021

CRISPR Technology for Breast Cancer: Diagnostics, Modeling, and Therapy
journal, August 2018

Combining orthogonal CRISPR and CRISPRi systems for genome engineering and metabolic pathway modulation in Escherichia coli
journal, February 2019

Attenuation of Inherited and Acquired Retinal Degeneration Progression with Gene-based Techniques
journal, December 2018

Orthogonal gene knockout and activation with a catalytically active Cas9 nuclease
journal, October 2015

Multiplexed labeling of genomic loci with dCas9 and engineered sgRNAs using CRISPRainbow
journal, April 2016

Partial DNA-guided Cas9 enables genome editing with reduced off-target activity
journal, January 2018

Hit and go CAS9 delivered through a lentiviral based self-limiting circuit
journal, May 2017

Editing the epigenome: technologies for programmable transcription and epigenetic modulation
journal, January 2016

A multifunctional AAV–CRISPR–Cas9 and its host response
journal, September 2016

Complex transcriptional modulation with orthogonal and inducible dCas9 regulators
journal, October 2016

Rapidly inducible Cas9 and DSB-ddPCR to probe editing kinetics
journal, July 2017

Genome-scale CRISPR-Cas9 knockout and transcriptional activation screening
journal, March 2017

Defining and improving the genome-wide specificities of CRISPR–Cas9 nucleases
journal, April 2016

Programmable DNA repair with CRISPRa/i enhanced homology-directed repair efficiency with a single Cas9
journal, July 2018

Combinatorial metabolic engineering using an orthogonal tri-functional CRISPR system
journal, November 2017

Site-specific manipulation of Arabidopsis loci using CRISPR-Cas9 SunTag systems
journal, February 2019

Multi-functional genome-wide CRISPR system for high throughput genotype–phenotype mapping
journal, December 2019

Rewiring of endogenous signaling pathways to genomic targets for therapeutic cell reprogramming
journal, January 2020

The emerging and uncultivated potential of CRISPR technology in plant science
journal, July 2019

Increasing the specificity of CRISPR systems with engineered RNA secondary structures
journal, April 2019

Multiplexed orthogonal genome editing and transcriptional activation by Cas12a
journal, December 2018

Multiplexed genome engineering by Cas12a and CRISPR arrays encoded on single transcripts
journal, August 2019

CRISPR RNA-guided autonomous delivery of Cas9
journal, December 2018

Precision Modulation of Neurodegenerative Disease-Related Gene Expression in Human iPSC-Derived Neurons
journal, June 2016

Graphene oxide-mediated Cas9/sgRNA delivery for efficient genome editing
journal, January 2018

A CRISPR/Cas9-based central processing unit to program complex logic computation in human cells
journal, March 2019

Transcriptional control by enhancers and enhancer RNAs
journal, October 2019

CRISPR-Cas9 nuclear dynamics and target recognition in living cells
journal, August 2016

The physicist’s guide to one of biotechnology’s hottest new topics: CRISPR-Cas
journal, April 2018

Recent advances in developing and applying biosensors for synthetic biology
journal, October 2019

Systematical study of the mechanistic factors regulating genome dynamics in vivo by CRISPRsie
journal, July 2019

Creation of versatile cloning platforms for transgene expression and dCas9-based epigenome editing
journal, December 2018

CRISPR-assisted multi-dimensional regulation for fine-tuning gene expression in Bacillus subtilis
journal, February 2019

PERSIST: A programmable RNA regulation platform using CRISPR endoRNases
preprint, December 2019

CRISPR Tools for Systematic Studies of RNA Regulation
journal, August 2019

A Model for Resource Competition in CRISPR-Mediated Gene Repression
conference, December 2018

A revolutionary tool: CRISPR technology plays an important role in construction of intelligentized gene circuits
journal, November 2018

Potential pitfalls of CRISPR/Cas9-mediated genome editing
journal, November 2015

Next stop for the CRISPR revolution: RNA-guided epigenetic regulators
journal, July 2016

Optimized paired-sgRNA/Cas9 cloning and expression cassette triggers high-efficiency multiplex genome editing in kiwifruit
journal, February 2018

Disabling Cas9 by an anti-CRISPR DNA mimic
journal, July 2017

Programming gene and engineered-cell therapies with synthetic biology
journal, February 2018

C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector
journal, June 2016

CRISPR-mediated activation of a promoter or enhancer rescues obesity caused by haploinsufficiency
journal, December 2018

A multiplex guide RNA expression system and its efficacy for plant genome engineering
journal, March 2020

Crossing enhanced and high fidelity SpCas9 nucleases to optimize specificity and cleavage
journal, October 2017

Multiplexed promoterless gene expression with CRISPReader
journal, June 2019

Modulating chromatin accessibility by transactivation and targeting proximal dsgRNAs enhances Cas9 editing efficiency in vivo
journal, July 2019

SWISS: multiplexed orthogonal genome editing in plants with a Cas9 nickase and engineered CRISPR RNA scaffolds
journal, June 2020

The Synergy between CRISPR and Chemical Engineering
journal, September 2019

Transgenic Mouse Models in Cancer Research
journal, July 2018

Gene activation by a CRISPR-assisted trans enhancer
journal, April 2019