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Citations to this article

Expanding the genetic editing tool kit: ZFNs, TALENs, and CRISPR-Cas9
Rajat M. Gupta, Kiran Musunuru
Rajat M. Gupta, Kiran Musunuru
Published October 1, 2014
Citation Information: J Clin Invest. 2014;124(10):4154-4161. https://doi.org/10.1172/JCI72992.
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Review Article has an altmetric score of 49

Expanding the genetic editing tool kit: ZFNs, TALENs, and CRISPR-Cas9

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Abstract

The past decade has been one of rapid innovation in genome-editing technology. The opportunity now exists for investigators to manipulate virtually any gene in a diverse range of cell types and organisms with targeted nucleases designed with sequence-specific DNA-binding domains. The rapid development of the field has allowed for highly efficient, precise, and now cost-effective means by which to generate human and animal models of disease using these technologies. This review will outline the recent development of genome-editing technology, culminating with the use of CRISPR-Cas9 to generate novel mammalian models of disease. While the road to using this same technology for treatment of human disease is long, the pace of innovation over the past five years and early successes in model systems build anticipation for this prospect.

Authors

Rajat M. Gupta, Kiran Musunuru

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Year: 2025 2024 2023 2022 2021 2020 2019 2018 2017 2016 2015 2009 Total
Citations: 5 32 23 32 28 24 19 14 14 14 12 1 218
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Journal of Advanced Research 2021
Correction of Muscular Dystrophies by CRISPR Gene Editing
Francesco Chemello, Rhonda Bassel-Duby, Eric N. Olson
Journal of Clinical Investigation 2020
Sharpening the Molecular Scissors: Advances in Gene-Editing Technology
M Broeders, P Herrero-Hernandez, MP Ernst, AT van der Ploeg, WW Pijnappel
iScience 2020
Lysosomal storage diseases: current therapies and future alternatives
AF Leal, AJ Espejo-Mojica, OF Sánchez, CM Ramírez, LH Reyes, JC Cruz, CJ Alméciga-Díaz
Journal of Molecular Medicine 2020
High level of fetal-globin reactivation by designed transcriptional activator-like effector
J Zhan, MJ Irudayam, Y Nakamura, R Kurita, AW Nienhuis
Blood Advances 2020
Novel genetic therapeutic approaches for modulating the severity of β‑thalassemia (Review)
F Amjad, T Fatima, T Fayyaz, M Khan, M Qadeer
Biomedical Reports 2020
Compensation of Disabled Organogeneses in Genetically Modified Pig Fetuses by Blastocyst Complementation
H Matsunari, M Watanabe, K Hasegawa, A Uchikura, K Nakano, K Umeyama, H Masaki, S Hamanaka, T Yamaguchi, M Nagaya, R Nishinakamura, H Nakauchi, H Nagashima
Stem Cell Reports 2020
The CRISP(Y) Future of Pediatric Soft Tissue Sarcomas
S Pomella, R Rota
Frontiers in Chemistry 2020
Human T cell glycosylation and implications on immune therapy for cancer
ED Bousser, L Meuris, N Callewaert, N Festjens
Human Vaccines & Immunotherapeutics 2020
Multigene CRISPR/Cas9 genome editing of hybrid proline rich proteins (HyPRPs) for sustainable multi-stress tolerance in crops: the review of a promising approach
B Saikia, S Singh, J Debbarma, N Velmurugan, H Dekaboruah, KP Arunkumar, C Chikkaputtaiah
Physiology and Molecular Biology of Plants 2020

How CRISPR-Cas System Could Be Used to Combat Antimicrobial Resistance


P Gholizadeh, Ş Köse, S Dao, K Ganbarov, A Tanomand, T Dal, M Aghazadeh, R Ghotaslou, MA Rezaee, B Yousefi, HS Kafil
Infection and drug resistance 2020
The clinical potential of gene editing as a tool to engineer cell-based therapeutics
C Ashmore-Harris, GO Fruhwirth
Clinical and Translational Medicine 2020
Progress and Challenges in the Improvement of Ornamental Plants by Genome Editing
CH Ahn, M Ramya, HR An, PM Park, YJ Kim, SY Lee, S Jang
Plants 2020
Advance genome editing technologies in the treatment of human diseases: CRISPR therapy (Review)
M Alagoz, N Kherad
International journal of molecular medicine 2020
Development of a Self-Restricting CRISPR-Cas9 System to Reduce Off-Target Effects
H Wang, H Lu, Y Lei, C Gong, Z Chen, Y Luan, Q Li, Y Jian, H Wang, F Wu, C Tao, H Shen, H Bo, H Shao, W Zhang
Molecular Therapy — Methods & Clinical Development 2020
Site-Specific Gene Knock-Out and On-Site Heterologous Gene Overexpression in Chlamydomonas reinhardtii via a CRISPR-Cas9-Mediated Knock-in Method
J Kim, S Lee, K Baek, ES Jin
Frontiers in Plant Science 2020

Nucleic Acid Therapy for β-Thalassemia


A d'Arqom
Biologics : targets & therapy 2020
Gene Therapy for Neurodegenerative Diseases: Slowing Down the Ticking Clock
R Martier, P Konstantinova
Frontiers in neuroscience 2020
Base editing: advances and therapeutic opportunities
EM Porto, AC Komor, IM Slaymaker, GW Yeo
Nature Reviews Drug Discovery 2020
A versatile toolkit for CRISPR-Cas13-based RNA manipulation in Drosophila
N Huynh, N Depner, R Larson, K King-Jones
Genome biology 2020
Genome Editing by CRISPR-Cas: A Game Change in the Genetic Manipulation of Chlamydomonas
M Ghribi, SB Nouemssi, F Meddeb-Mouelhi, I Desgagné-Penix
Life Sciences 2020
CRISPR FokI Dead Cas9 System: Principles and Applications in Genome Engineering
M Saifaldeen, DE Al-Ansari, D Ramotar, M Aouida
Cells 2020
Various Aspects of a Gene Editing System—CRISPR–Cas9
E Janik, M Niemcewicz, M Ceremuga, L Krzowski, J Saluk-Bijak, M Bijak
International journal of molecular sciences 2020
Novel insights into gene therapy in the cornea
RR Mohan, LM Martin, NR Sinha
Experimental Eye Research 2020
Targeting of cholera toxin A (ctxA) gene by zinc finger nuclease: pitfalls of using gene editing tools in prokaryotes
N Hosseini, H Khanahmad, BN Esfahani, M Bandehpour, L Shariati, N Zahedi, B Kazemi
Research in Pharmaceutical Sciences 2020
Gene therapy of hematological disorders: current challenges
AM Al-Saif
Gene Therapy 2019
Programmable Molecular Scissors: Applications of a New Tool for Genome Editing in Biotech
SK Saha, FK Saikot, S Rahman, MA Jamal, SM Rahman, SM Islam, KH Kim
Molecular Therapy — Nucleic Acids 2019
hiPSCs in cardio-oncology: deciphering the genomics
EA Pinheiro, KA Fetterman, PW Burridge
Cardiovascular Research 2019
Targeting Telomeres and Telomerase: Studies in Aging and Disease Utilizing CRISPR/Cas9 Technology
A Brane, T Tollefsbol
Cells 2019
Use of Genome Editing Tools in Environmental Health Research
JE Rager, C Carberry, RC Fry
Current Opinion in Toxicology 2019
An update on the tools for creating transgenic animal models of human diseases – focus on atherosclerosis
AS Volobueva, AN Orekhov, AV Deykin
Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas / Sociedade Brasileira de Biofisica ... [et al.] 2019
New Human Chromosomal Sites with “Safe Harbor” Potential for Targeted Transgene Insertion
S Pellenz, M Phelps, W Tang, BT Hovde, RB Sinit, W Fu, H Li, E Chen, RJ Monnat
Human Gene Therapy 2019
Public attitudes towards genetically modified polled cattle
E McConnachie, MJ Hötzel, JA Robbins, A Shriver, DM Weary, MA von Keyserlingk, IA Olsson
PloS one 2019
An Overview Of The Crispr-Based Genomic- And Epigenome-Editing System: Function, Applications, And Challenges
SB Qomi, A Asghari, M Mojarrad
Advanced Biomedical Research 2019
Transgenerational Perpetuation of CHS Gene Expression and DNA Methylation Status Induced by Short Oligodeoxynucleotides in Flax (Linum usitatissimum)
M Dzialo, J Szopa, A Hnitecka, M Zuk
International journal of molecular sciences 2019
Sheep and Goat Genome Engineering: From Random Transgenesis to the CRISPR Era
P Kalds, S Zhou, B Cai, J Liu, Y Wang, B Petersen, T Sonstegard, X Wang, Y Chen
Frontiers in Genetics 2019
Era of Genomic Medicine: A Narrative Review on CRISPR Technology as a Potential Therapeutic Tool for Human Diseases
OW Kotagama, CD Jayasinghe, T Abeysinghe
BioMed Research International 2019
Gene surgery: Potential applications for human diseases
Ayman El-Kenawy, Bachir Benarba, Adriana Freitas Neves, Thaise Gonçalves de Araujo, Bee Ling Tan, Adel Gouri
EXCLI J 2019
The Scope for Thalassemia Gene Therapy by Disruption of Aberrant Regulatory Elements
P Patsali, C Mussolino, P Ladas, A Floga, A Kolnagou, S Christou, M Sitarou, MN Antoniou, T Cathomen, CW Lederer, M Kleanthous
Journal of Clinical Medicine 2019
The potential of genomics for restoring ecosystems and biodiversity
MF Breed, PA Harrison, C Blyth, M Byrne, V Gaget, NJ Gellie, SV Groom, R Hodgson, JG Mills, TA Prowse, DA Steane, JJ Mohr
Nature Reviews Genetics 2019
Climatic changes and potatoes: How can we cope with the abiotic stresses?
T Handayani, SA Gilani, KN Watanabe
Breeding Science 2019
Zebrafish In Vivo Models of Cancer and Metastasis
KR Astell, D Sieger
Cold Spring Harbor Perspectives in Medicine 2019
Synthetic microbial consortia for biosynthesis and biodegradation: promises and challenges
S Che, Y Men
Journal of Industrial Microbiology & Biotechnology 2019
Evaluation of the CRISPR/Cas9 directed mutant TP53 gene repairing effect in human prostate cancer cell line PC-3
MB Batır, E Şahin, FS Çam
Molecular Biology Reports 2019
Gene Editing and Gene-Based Therapeutics for Cardiomyopathies
JC Ohiri, EM McNally
Heart Failure Clinics 2018
Molecular Evidence of Genome Editing in a Mouse Model of Immunodeficiency
HH Abdul-Razak, CJ Rocca, SJ Howe, ME Alonso-Ferrero, J Wang, R Gabriel, CC Bartholomae, CH Gan, MI Garín, A Roberts, MP Blundell, V Prakash, FJ Molina-Estevez, J Pantoglou, G Guenechea, MC Holmes, PD Gregory, C Kinnon, C von Kalle, M Schmidt, JA Bueren, AJ Thrasher, RJ Yáñez-Muñoz
Scientific Reports 2018
Delivering CRISPR: a review of the challenges and approaches
CA Lino, JC Harper, JP Carney, JA Timlin
Drug Delivery 2018
Knocking out Ornithine Decarboxylase Antizyme 1 (OAZ1) Improves Recombinant Protein Expression in the HEK293 Cell Line
L Abaandou, J Shiloach
Medical Sciences 2018
Zebrafish as a model for kidney function and disease
P Outtandy, C Russell, R Kleta, D Bockenhauer
Pediatric Nephrology 2018
Progress in Gene Therapy to Prevent Retinal Ganglion Cell Loss in Glaucoma and Leber’s Hereditary Optic Neuropathy
SE Ratican, A Osborne, KR Martin
Neural plasticity 2018
CRISPR/Cas9 genome surgery for retinal diseases
CL Xu, KS Park, SH Tsang
Drug discovery today. Technologies 2018
The Potential of CRISPR/Cas9 Gene Editing as a Treatment Strategy for Alzheimer's Disease
TT Rohn, N Kim, NF Isho, JM Mack
Journal of Alzheimer's disease & Parkinsonism 2018
Evolution of the SPX gene family in plants and its role in the response mechanism to phosphorus stress
N Liu, W Shang, C Li, L Jia, X Wang, G Xing, WM Zheng
Open Biology 2018
In vivo epigenome editing and transcriptional modulation using CRISPR technology
CH Lau, Y Suh
Transgenic Research 2018
Genome Editing: A New Horizon for Oral and Craniofacial Research
N Yu, J Yang, Y Mishina, WV Giannobile
Journal of dental research 2018
A Drosophila CRISPR/Cas9 Toolkit for Conditionally Manipulating Gene Expression in the Prothoracic Gland as a Test Case for Polytene Tissues
N Huynh, J Zeng, W Liu, K King-Jones
G3: Genes|Genomes|Genetics 2018
Current progress in CRISPR‐based diagnostic platforms
K Khambhati, G Bhattacharjee, V Singh
Journal of Cellular Biochemistry 2018
The road less traveled: strategies to enhance the frequency of homology-directed repair (HDR) for increased efficiency of CRISPR/Cas-mediated transgenesis
Devkota S
BMB Reports 2018
Atherogenesis and Metabolic Dysregulation in LDL Receptor Knockout Rats
Srinivas Dwarakanath Sithu, Marina V. Malovichko, Krista A Riggs, Nalinie S Wickramasinghe, Millicent G Winner, Abhinav Agarwal, Rihab E Hamed-Berair, Anuradha Kalani, Daniel W Riggs, Aruni Bhatnagar, Sanjay Srivastava
JCI Insight 2017
Transcriptional control of chondrocyte specification and differentiation
CF Liu, WE Samsa, G Zhou, V Lefebvre
Seminars in Cell & Developmental Biology 2017
The Impact of CRISPR/Cas9 Technology on Cardiac Research: From Disease Modelling to Therapeutic Approaches
BM Motta, PP Pramstaller, AA Hicks, A Rossini
Stem Cells International 2017
Genome Editing and Muscle Stem Cells as a Therapeutic Tool for Muscular Dystrophies
V Pini, JE Morgan, F Muntoni, HC ONeill
Current Stem Cell Reports 2017
CRISPR/Cas9: Transcending the Reality of Genome Editing
S Chira, D Gulei, A Hajitou, AA Zimta, P Cordelier, I Berindan-Neagoe
Molecular Therapy - Nucleic Acids 2017
Frameshift indels introduced by genome editing can lead to in-frame exon skipping
S Lalonde, OA Stone, S Lessard, A Lavertu, J Desjardins, M Beaudoin, M Rivas, DY Stainier, G Lettre, AS Lewin
PloS one 2017
Drugs in Development for Hepatitis B
A Dawood, SA Basit, M Jayaraj, RG Gish
Drugs 2017
Oligo- and dsDNA-mediated genome editing using a tetA dual selection system in Escherichia coli
YS Ryu, SP Chandran, K Kim, SK Lee, M Isalan
PloS one 2017
Human Germline Genome Editing
KE Ormond, DP Mortlock, DT Scholes, Y Bombard, LC Brody, WA Faucett, NA Garrison, L Hercher, R Isasi, A Middleton, K Musunuru, D Shriner, A Virani, CE Young
The American Journal of Human Genetics 2017
Self-cleaving ribozymes enable the production of guide RNAs from unlimited choices of promoters for CRISPR/Cas9 mediated genome editing
Y He, T Zhang, N Yang, M Xu, L Yan, L Wang, R Wang, Y Zhao
Journal of Genetics and Genomics 2017
Genome Editing
K Musunuru
Journal of the American College of Cardiology 2017
Producing defucosylated antibodies with enhanced in vitro antibody-dependent cellular cytotoxicity via FUT8 knockout CHO-S cells
H Zong, L Han, K Ding, J Wang, T Sun, X Zhang, C Cagliero, H Jiang, Y Xie, J Xu, B Zhang, J Zhu
Engineering in Life Sciences 2017
The next generation of antimicrobial peptides (AMPs) as molecular therapeutic tools for the treatment of diseases with social and economic impacts
NB da Cunha, NB Cobacho, JF Viana, LA Lima, KB Sampaio, SS Dohms, AC Ferreira, C de la Fuente-Núñez, FF Costa, OL Franco, SC Dias
Drug Discovery Today 2017
Recent Advances in Nucleic Acid Targeting Probes and Supramolecular Constructs Based on Pyrene-Modified Oligonucleotides.
Krasheninina OA, Novopashina DS, Apartsin EK, Venyaminova AG
Molecules (Basel, Switzerland) 2017
Emerging cellular and gene therapies for congenital anemias: Emerging Cellular and Gene Therapies for Congenital
LS Ludwig, RK Khajuria, VG Sankaran
American Journal of Medical Genetics Part C Seminars in Medical Genetics 2016
Genetics and Genomics of Coronary Artery Disease
M Pjanic, CL Miller, R Wirka, JB Kim, DM DiRenzo, T Quertermous
Current Cardiology Reports 2016
Gene Editing of Human Hematopoietic Stem and Progenitor Cells: Promise and Potential Hurdles
KR Yu, H Natanson, CE Dunbar
Human Gene Therapy 2016
Development and potential applications of CRISPR-Cas9 genome editing technology in sarcoma
T Liu, JK Shen, Z Li, E Choy, FJ Hornicek, Z Duan
Cancer Letters 2016
The Gene Targeting Approach of Small Fragment Homologous Replacement (SFHR) Alters the Expression Patterns of DNA Repair and Cell Cycle Control Genes
S Pierandrei, A Luchetti, M Sanchez, G Novelli, F Sangiuolo, M Lucarelli
Molecular Therapy — Nucleic Acids 2016
Harnessing the Prokaryotic Adaptive Immune System as a Eukaryotic Antiviral Defense
AA Price, A Grakoui, DS Weiss
Trends in Microbiology 2016
Genome editing in cardiovascular diseases
A Strong, K Musunuru
Nature Reviews Cardiology 2016
CT-Finder: A Web Service for CRISPR Optimal Target Prediction and Visualization
H Zhu, L Misel, M Graham, ML Robinson, C Liang
Scientific Reports 2016
Detection of nucleotide-specific CRISPR/Cas9 modified alleles using multiplex ligation detection
R KC, A Srivastava, JM Wilkowski, CE Richter, JA Shavit, DT Burke, SL Bielas
Scientific Reports 2016
A Broad Overview and Review of CRISPR-Cas Technology and Stem Cells
SN Waddington, R Privolizzi, R Karda, HC ONeill
Current Stem Cell Reports 2016
A 90-Day Feeding Study in Rats to Assess the Safety of Genetically Engineered Pork
G Xiao, SW Jiang, LL Qian, CB Cai, Q Wang, DZ Ma, B Li, S Xie, WT Cui, K Li, M Bader
PloS one 2016
Efficient, footprint-free human iPSC genome editing by consolidation of Cas9/CRISPR and piggyBac technologies
G Wang, L Yang, D Grishin, X Rios, LY Ye, Y Hu, K Li, D Zhang, GM Church, WT Pu
Nature Protocols 2016
Novel Thrombotic Function of a Human SNP in STXBP5 Revealed by CRISPR/Cas9 Gene Editing in MiceHighlights
QM Zhu, KA Ko, S Ture, MA Mastrangelo, MH Chen, AD Johnson, CJ ODonnell, CN Morrell, JM Miano, CJ Lowenstein
Arteriosclerosis, thrombosis, and vascular biology 2016
Cure for thalassemia major – from allogeneic hematopoietic stem cell transplantation to gene therapy
A Srivastava, RV Shaji
Haematologica 2016
Society for Pediatric Research 2015 Young Investigator Award: genetics of human hematopoiesis—what patients can teach us about blood cell production
A Wakabayashi, VG Sankaran
Pediatric Research 2015
Anemia: progress in molecular mechanisms and therapies
VG Sankaran, MJ Weiss
Nature Medicine 2015
Targeted Application of Human Genetic Variation Can Improve Red Blood Cell Production from Stem Cells
FC Giani, C Fiorini, A Wakabayashi, LS Ludwig, RM Salem, CD Jobaliya, SN Regan, JC Ulirsch, G Liang, O Steinberg-Shemer, MH Guo, T Esko, W Tong, C Brugnara, JN Hirschhorn, MJ Weiss, LI Zon, ST Chou, DL French, K Musunuru, VG Sankaran
Cell Stem Cell 2015
Progress and Prospects of Anti-HBV Gene Therapy Development
M Maepa, I Roelofse, A Ely, P Arbuthnot
International journal of molecular sciences 2015
Zebrafish as a disease model for studying human hepatocellular carcinoma
JW Lu
World journal of gastroenterology : WJG 2015
Genome engineering in cattle: recent technological advancements
Z Wang
Chromosome Research 2015
Toward stem cell-based phenotypic screens for neurodegenerative diseases
V Khurana, DF Tardiff, CY Chung, S Lindquist
Nature Reviews Neurology 2015
Chromatin organization in pluripotent cells: emerging approaches to study and disrupt function
CL Novo, PJ Rugg-Gunn
Briefings in Functional Genomics 2015
Plant artificial chromosome technology and its potential application in genetic engineering
W Yu, YY Yau, JA Birchler
Plant Biotechnology Journal 2015
2015 Guidelines for Establishing Genetically Modified Rat Models for Cardiovascular Research
MJ Flister, JW Prokop, J Lazar, M Shimoyama, M Dwinell, A Geurts
Journal of Cardiovascular Translational Research 2015
Neurology—the next 10 years
R Baron, DM Ferriero, GB Frisoni, C Bettegowda, ZL Gokaslan, JA Kessler, A Vezzani, SG Waxman, S Jarius, B Wildemann, M Weller
Nature Reviews Neurology 2015
Animal and human mucosal tissue models to study HIV biomedical interventions: can we predict success?
Dezzutti CS
Journal of the International AIDS Society 2015
Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology 2009

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