Cited by 549Hemophilia Treatment and ResearchCRISPR and Genetic EngineeringVirus-based gene therapy research

The DOI matches its Crossref record; 29 of the 29 references it cites were found in a registry or an index.

In vivo genome editing restores haemostasis in a mouse model of haemophilia

Open access

Li, Hojun, Haurigot, Virginia, Doyon, Yannick, Li, Tianjian, Wong, Sunnie Y., Bhagwat, Anand S., Malani, Nirav, Anguela, Xavier M., Sharma, Rajiv, Ivanciu, Lacramiora, Murphy, Samuel L., Finn, Jonathan D., Khazi, Fayaz R., Zhou, Shangzhen, Paschon, David E., Rebar, Edward J., Bushman, Frederic D., Gregory, Philip D., Holmes, Michael C., High, Katherine A.·2011·Nature

DOI 10.1038/nature10177PMC PMC3152293

Open this paper in CoChat — free account

Abstract

Editing of the human genome to correct disease-causing mutations is a promising approach for the treatment of genetic disorders. Genome editing improves on simple gene-replacement strategies by effecting in situ correction of a mutant gene, thus restoring normal gene function under the control of endogenous regulatory elements and reducing risks associated with random insertion into the genome. Gene-specific targeting has historically been limited to mouse embryonic stem cells. The development of zinc finger nucleases (ZFNs) has permitted efficient genome editing in transformed and primary cells that were previously thought to be intractable to such genetic manipulation. In vitro, ZFNs have been shown to promote efficient genome editing via homology-directed repair by inducing a site-specific double-strand break (DSB) at a target locus, but it is unclear whether ZFNs can induce DSBs and stimulate genome editing at a clinically meaningful level in vivo. Here we show that ZFNs are able to induce DSBs efficiently when delivered directly to mouse liver and that, when co-delivered with an appropriately designed gene-targeting vector, they can stimulate gene replacement through both homology-directed and homology-independent targeted gene insertion at the ZFN-specified locus. The level of gene targeting achieved was sufficient to correct the prolonged clotting times in a mouse model of haemophilia B, and remained persistent after induced liver regeneration. Thus, ZFN-driven gene correction can be achieved in vivo, raising the possibility of genome editing as a viable strategy for the treatment of genetic disease.

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

Crossref · 10.1038/nature10177

Cites

29 of 29 references verified0 citation errors · 0 not checkable

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.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The Metabolic and Molecular Bases of Inherited Disease
Scriver, R. C. (1995) · Medical Entomology and Zoology · Cited by 12,101
LMO2 -Associated Clonal T Cell Proliferation in Two Patients after Gene Therapy for SCID-X1
Hacein-Bey-Abina, S., Von Kalle, C., Schmidt, M., McCormack, M. P., Wulffraat, N., Leboulch, P., Lim, A., Osborne, C. S., Pawliuk, R., Morillon, E., et al. (2003) · Science · doi:10.1126/science.1088547 · Cited by 3,587
Genome editing with engineered zinc finger nucleases
Urnov, F. D., Rebar, E. J., Holmes, M. C., Zhang, H. S., & Gregory, P. D. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2842 · Cited by 2,285
Self-citation
Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response
Manno, C. S., Pierce, G. F., Arruda, V. R., Glader, B., Ragni, M., Rasko, J. J. E., Ozelo, M. C., Hoots, K., Blatt, P., Konkle, B., et al. (2006) · Nature Medicine · doi:10.1038/nm1358 · Cited by 2,163
Self-citation
Safety and Efficacy of Gene Transfer for Leber's Congenital Amaurosis
Maguire, A. M., Simonelli, F., Pierce, E. A., Pugh, E. N., Mingozzi, F., Bennicelli, J., Banfi, S., Marshall, K. A., Testa, F., Surace, E. M., et al. (2008) · New England Journal of Medicine · doi:10.1056/nejmoa0802315 · Cited by 2,145
Self-citation
Effect of gene therapy on visual function in Leber’s congenital amaurosis
Bainbridge, J. W. B., Smith, A. J., Barker, S. S., Robbie, S., Henderson, R., Balaggan, K., Viswanathan, A., Holder, G. E., Stockman, A., Tyler, N., et al. (2008) · New England Journal of Medicine · doi:10.1056/nejmoa0802268 · Cited by 1,924
Highly efficient endogenous human gene correction using designed zinc-finger nucleases
Urnov, F. D., Miller, J. C., Lee, Y.-L., Beausejour, C. M., Rock, J. M., Augustus, S., Jamieson, A. C., Porteus, M. H., Gregory, P. D., & Holmes, M. C. (2005) · Nature · doi:10.1038/nature03556 · Cited by 1,642
Self-citation
Treatment of Sickle Cell Anemia Mouse Model with iPS Cells Generated from Autologous Skin
Hanna, J. H., Wernig, M., Markoulaki, S., Sun, C., Meissner, A., Cassady, J. P., Beard, C., Brambrink, T., Wu, L.-C., Townes, T. M., et al. (2007) · Science · doi:10.1126/science.1152092 · Cited by 1,521
Hematopoietic Stem Cell Gene Therapy with a Lentiviral Vector in X-Linked Adrenoleukodystrophy
Cartier, N., Hacein-Bey-Abina, S., Bartholomae, C. C., Veres, G., Schmidt, M., Kutschera, I., Vidaud, M., Abel, U., Dal-Cortivo, L., Caccavelli, L., et al. (2009) · Science · doi:10.1126/science.1171242 · Cited by 1,508
Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients
Howe, S. J., Mansour, M. R., Schwarzwaelder, K., Bartholomae, C., Hubank, M., Kempski, H., Brugman, M. H., Pike-Overzet, K., Chatters, S. J., de Ridder, D., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci35798 · Cited by 1,286

Show all 29 references

Sorted by citations

Items 101–200 of 549

Development of hybrid viral vectors for gene therapy
Huang, S., & Kamihira, M. (2012) · Biotechnology Advances · doi:10.1016/j.biotechadv.2012.10.001 · Cited by 102
Gene Therapy for Hemophilia
Nienhuis, A. W., Nathwani, A. C., & Davidoff, A. M. (2017) · Molecular Therapy · doi:10.1016/j.ymthe.2017.03.033 · Cited by 103
Ready for Repair? Gene Editing Enters the Clinic for the Treatment of Human Disease
Ernst, M. P. T., Broeders, M., Herrero-Hernandez, P., Oussoren, E., van der Ploeg, A. T., & Pijnappel, W. W. M. P. (2020) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2020.06.022 · Cited by 103
In Vivo Delivery Systems for Therapeutic Genome Editing
Wang, L., Li, F., Dang, L., Liang, C., Wang, C., He, B., Liu, J., Li, D., Wu, X., Xu, X., et al. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17050626 · Cited by 101
Gene therapy for hemophilia: what does the future hold?
Doshi, B. S., & Arruda, V. R. (2018) · Therapeutic Advances in Hematology · doi:10.1177/2040620718791933 · Cited by 101
Evaluating risks of insertional mutagenesis by DNA transposons in gene therapy
Hackett, P. B., Largaespada, D. A., Switzer, K. C., & Cooper, L. J. N. (2013) · Translational research · doi:10.1016/j.trsl.2012.12.005 · Cited by 97
Non-viral Delivery of Zinc Finger Nuclease mRNA Enables Highly Efficient In Vivo Genome Editing of Multiple Therapeutic Gene Targets
Conway, A., Mendel, M., Kim, K., McGovern, K., Boyko, A., Zhang, L., Miller, J. C., DeKelver, R. C., Paschon, D. E., Mui, B. L., et al. (2019) · Molecular Therapy · doi:10.1016/j.ymthe.2019.03.003 · Cited by 95
Self-citation
A Molecular Revolution in the Treatment of Hemophilia
Butterfield, J. S. S., Hege, K. M., Herzog, R. W., & Kaczmarek, R. (2019) · Molecular Therapy · doi:10.1016/j.ymthe.2019.11.006 · Cited by 97
Genomically humanized mice: technologies and promises
Devoy, A., Bunton-Stasyshyn, R. K. A., Tybulewicz, V. L. J., Smith, A. J. H., & Fisher, E. (2011) · Nature Reviews Genetics · doi:10.1038/nrg3116 · Cited by 93
Ribosomal and hematopoietic defects in induced pluripotent stem cells derived from Diamond Blackfan anemia patients
Garçon, L., Ge, J., Manjunath, S. H., Mills, J. A., Apicella, M., Parikh, S. P., Sullivan, L. M., Podsakoff, G. M., Gadue, P. J., French, D. L., et al. (2013) · Blood · doi:10.1182/blood-2013-01-478321 · Cited by 92
Gene targeting to the ROSA26 locus directed by engineered zinc finger nucleases
Pérez‐Piñera, P., Ousterout, D. G., Brown, M. T., & Gersbach, C. A. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1214 · Cited by 92
Long-term correction of hemophilia B using adenoviral delivery of CRISPR/Cas9
Stephens, C. J., Lauron, E. J., Kashentseva, E. A., Lu, Z. H., Yokoyama, W. M., & Curiel, D. T. (2019) · Journal of Controlled Release · doi:10.1016/j.jconrel.2019.02.009 · Cited by 89
CRISPR/Cas9-mediated glycolate oxidase disruption is an efficacious and safe treatment for primary hyperoxaluria type I
Zabaleta, N., Barberia, M., Martín-Higueras, C., Zapata‐Linares, N., Betancor, I., Rodríguez-Diaz, S., Martínez-Turrillas, R., Torella, L., Vales, Á., Olagüe, C., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07827-1 · Cited by 86
CRISPR/Cas9-mediated in vivo gene targeting corrects hemostasis in newborn and adult factor IX–knockout mice
Wang, L., Yang, Y., Breton, C. A., White, J., Zhang, J., Che, Y., Saveliev, A., McMenamin, D., He, Z., Latshaw, C., et al. (2019) · Blood · doi:10.1182/blood.2019000790 · Cited by 85
ZFN-mediated in vivo genome editing corrects murine hurler syndrome
Ou, L., DeKelver, R. C., Rohde, M., Tom, S., Radeke, R., St. Martin, S. J., Santiago, Y., Sproul, S., Przybilla, M. J., Koniar, B. L., et al. (2019) · Molecular Therapy · doi:10.1016/j.ymthe.2018.10.018 · Cited by 84
Self-citation
State-of-the-art human gene therapy: part II. Gene therapy strategies and clinical applications.
Wang, D., & Gao, G. (2014) · PubMed · Cited by 84
Correction of the ΔF508 Mutation in the Cystic Fibrosis Transmembrane Conductance Regulator Gene by Zinc-Finger Nuclease Homology-Directed Repair
Lee, C. M., Flynn, R., Hollywood, J. A., Scallan, M. F., & Harrison, P. T. (2012) · BioResearch open access · doi:10.1089/biores.2012.0218 · Cited by 89
Zinc-finger nuclease-mediated gene correction using single AAV vector transduction and enhancement by Food and Drug Administration-approved drugs
Ellis, B. L., Hirsch, M. L., Porter, S. N., Samulski, R. J., & Porteus, M. H. (2012) · Gene Therapy · doi:10.1038/gt.2011.211 · Cited by 85
iGUIDE: an improved pipeline for analyzing CRISPR cleavage specificity
Nobles, C. L., Reddy, S. G., Salas-McKee, J., Liu, X., June, C. H., Melenhorst, J. J., Suhoski, M. M., Zhao, Y., & Bushman, F. D. (2019) · Genome biology · doi:10.1186/s13059-019-1625-3 · Cited by 82
Self-citation
Zinc finger nucleases: looking toward translation
Palpant, N. J., & Dudzinski, D. M. (2012) · Gene Therapy · doi:10.1038/gt.2012.2 · Cited by 82
CRISPR/Cas9: a powerful tool for identification of new targets for cancer treatment
Liu, B., Saber, A., & Haisma, H. J. (2019) · Drug Discovery Today · doi:10.1016/j.drudis.2019.02.011 · Cited by 86
Hematopoietic stem cell engineering at a crossroads
Rivière, I., Dunbar, C. E., & Sadelain, M. (2011) · Blood · doi:10.1182/blood-2011-09-349993 · Cited by 80
Systemic delivery of triplex-forming PNA and donor DNA by nanoparticles mediates site-specific genome editing of human hematopoietic cells in vivo
McNeer, N. A., Schleifman, E., Cuthbert, A., Brehm, M. A., Jackson, A. M., Cheng, C., Anandalingam, K. K., Kumar, P., Shultz, L. D., Greiner, D. L., et al. (2012) · Gene Therapy · doi:10.1038/gt.2012.82 · Cited by 79
In Vivo Genome Editing as a Therapeutic Approach
Ho, B. X., Loh, S. J. H., Chan, W., & Soh, B.-S. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19092721 · Cited by 81
Prelamin A causes progeria through cell-extrinsic mechanisms and prevents cancer invasion
Rosa, J. D. L., Freije, J. M. P., Cabanillas, R., Osorio, F. G., Fraga, M. F., Fernández-García, M. S., Rad, R., Fanjul, V., Ugalde, A. P., Liang, Q., et al. (2013) · Nature Communications · doi:10.1038/ncomms3268 · Cited by 79
Full-length dystrophin restoration via targeted exon integration by AAV-CRISPR in a humanized mouse model of Duchenne muscular dystrophy
Pickar‐Oliver, A., Gough, V., Bohning, J. D., Liu, S., Robinson-Hamm, J. N., Daniels, H., Majoros, W. H., Devlin, G. W., Asokan, A., & Gersbach, C. A. (2021) · Molecular Therapy · doi:10.1016/j.ymthe.2021.09.003 · Cited by 78
Rescue of bilirubin‐induced neonatal lethality in a mouse model of Crigler‐Najjar syndrome type I by AAV9‐mediated gene transfer
Bortolussi, G., Zentilin, L., Baj, G., Giraudi, P. J., Bellarosa, C., Giacca, M., Tiribelli, C., & Muro, A. F. (2011) · The FASEB Journal · doi:10.1096/fj.11-195461 · Cited by 75
CRISPR/Cas9-mediated somatic and germline gene correction to restore hemostasis in hemophilia B mice
Huai, C., Jia, C., Sun, R., Xu, P., Min, T., Wang, Q., Zheng, C., Chen, H., & Lu, D. (2017) · Human Genetics · doi:10.1007/s00439-017-1801-z · Cited by 76
AAV Gene Transfer with Tandem Promoter Design Prevents Anti-transgene Immunity and Provides Persistent Efficacy in Neonate Pompe Mice
Colella, P., Sellier, P., Verdera, H. C., Puzzo, F., van Wittenberghe, L., Guerchet, N., Danièle, N., Gjata, B., Marmier, S., Charles, S., et al. (2018) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2018.11.002 · Cited by 78
Versatile and robust genome editing with Streptococcus thermophilus CRISPR1-Cas9Preprint
Agudelo, D., Carter, S., Velimirovic, M., Duringer, A., Rivest, J.-F., Levesque, S., Loehr, J., Mouchiroud, M., Cyr, D., Waters, P. J., et al. (2020) · Genome Research · doi:10.1101/gr.255414.119 · Cited by 75
Self-citation
Adeno-associated viral vectors for the treatment of hemophilia
High, K. A., & Anguela, X. M. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv475 · Cited by 77
Self-citation
Genome engineering: a new approach to gene therapy for neuromuscular disorders
Nelson, C. E., Robinson-Hamm, J. N., & Gersbach, C. A. (2017) · Nature Reviews Neurology · doi:10.1038/nrneurol.2017.126 · Cited by 73
Development of gene transfer for induction of antigen-specific tolerance
Sack, B. K., Herzog, R. W., Terhorst, C., & Markusic, D. M. (2014) · Molecular Therapy - Methods & Clinical Development · doi:10.1038/mtm.2014.13 · Cited by 70
Curing hemophilia A by NHEJ-mediated ectopic F8 insertion in the mouse
Zhang, J., Cheng, X., Zhao, M., Li, G., Xu, J., Zhang, F., Yin, M., Meng, F., Dai, X., Fu, Y.-W., et al. (2019) · Genome biology · doi:10.1186/s13059-019-1907-9 · Cited by 73
A translationally optimized AAV-UGT1A1 vector drives safe and long-lasting correction of Crigler-Najjar syndrome
Ronzitti, G., Bortolussi, G., van Dijk, R., Collaud, F., Charles, S., Leborgne, C., Vidal, P., Martin, S., Gjata, B., Sola, M. S., et al. (2016) · Molecular Therapy — Methods & Clinical Development · doi:10.1038/mtm.2016.49 · Cited by 72
Towards a new era in medicine: therapeutic genome editing
Porteus, M. H. (2015) · Genome Biology · doi:10.1186/s13059-015-0859-y · Cited by 69
Gene therapies that restore dystrophin expression for the treatment of Duchenne muscular dystrophy
Robinson-Hamm, J. N., & Gersbach, C. A. (2016) · Human Genetics · doi:10.1007/s00439-016-1725-z · Cited by 72
Precise in vivo genome editing via single homology arm donor mediated intron-targeting gene integration for genetic disease correction
Suzuki, K., Yamamoto, M., Hernández‐Benítez, R., Li, Z., Wei, C., Soligalla, R. D., Aizawa, E., Hatanaka, F., Kurita, M., Reddy, P., et al. (2019) · Cell Research · doi:10.1038/s41422-019-0213-0 · Cited by 69
Genome Editing B.C. (Before CRISPR): Lasting Lessons from the “Old Testament”
Urnov, F. D. (2018) · The CRISPR Journal · doi:10.1089/crispr.2018.29007.fyu · Cited by 71
Evolving AAV-delivered therapeutics towards ultimate cures
He, X., Urip, B. A., Zhang, Z., Ngan, C. C., & Feng, B. (2021) · Journal of Molecular Medicine · doi:10.1007/s00109-020-02034-2 · Cited by 70
Animal Models of Hemophilia
Sabatino, D. E., Nichols, T. C., Merricks, E. P., Bellinger, D. A., Herzog, R. W., & Monahan, P. E. (2011) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-394596-9.00006-8 · Cited by 68
Oligonucleotide-based strategies to combat polyglutamine diseases
Fiszer, A., & Krzyżosiak, W. J. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku385 · Cited by 70
Designed nucleases for targeted genome editing
Lee, J., Chung, J., Kim, H. M., Kim, S., & Kim, S. (2015) · Plant Biotechnology Journal · doi:10.1111/pbi.12465 · Cited by 70
A mutation-independent CRISPR-Cas9–mediated gene targeting approach to treat a murine model of ornithine transcarbamylase deficiency
Wang, L., Yang, Y., Breton, C. A., Bell, P. L., Li, M., Zhang, J., Che, Y., Saveliev, A., He, Z., White, J., et al. (2020) · Science Advances · doi:10.1126/sciadv.aax5701 · Cited by 67
Integrase-defective Lentiviral Vectors as a Delivery Platform for Targeted Modification of Adenosine Deaminase Locus
Joglekar, A. V., Hollis, R. P., Kuftinec, G., Senadheera, S., Chan, R., & Kohn, D. B. (2013) · Molecular Therapy · doi:10.1038/mt.2013.106 · Cited by 65
Gene Correction of a Duchenne Muscular Dystrophy Mutation by Meganuclease-Enhanced Exon Knock-In
Popplewell, L. J., Koo, T., Leclerc, X., Duclert, A., Mamchaoui, K., Gouble, A., Mouly, V., Voït, T., Pâques, F., Cédrone, F., et al. (2013) · Human Gene Therapy · doi:10.1089/hum.2013.081 · Cited by 69
Engineered Nanomaterials to Potentiate CRISPR/Cas9 Gene Editing for Cancer Therapy
Yi, K., Kong, H., Lao, Y., Li, D., Mintz, R. L., Fang, T., Chen, G., Tao, Y., Li, M., & Ding, J. (2023) · Advanced Materials · doi:10.1002/adma.202300665 · Cited by 66
Versatile and Efficient Genome Editing in Human Cells by Combining Zinc-Finger Nucleases With Adeno-Associated Viral Vectors
Händel, E.-M., Gellhaus, K., Khan, K., Bednarski, C., Cornu, T. I., Müller-Lerch, F., Kotin, R. M., Heilbronn, R., & Cathomen, T. (2011) · Human Gene Therapy · doi:10.1089/hum.2011.140 · Cited by 66
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
Delivering on the promise of gene editing for cystic fibrosis
Hodges, C. A., & Conlon, R. A. (2018) · Genes & Diseases · doi:10.1016/j.gendis.2018.11.005 · Cited by 63
Hemophilia gene therapy comes of age
George, L. A. (2017) · Blood Advances · doi:10.1182/bloodadvances.2017009878 · Cited by 63
Customizing the genome as therapy for the β-hemoglobinopathies.
Canver, M. C., & Orkin, S. H. (2016) · Blood · doi:10.1182/blood-2016-01-678128 · Cited by 61
Human Pluripotent Stem Cells for Modelling Human Liver Diseases and Cell Therapy
Dianat, N., Steichen, C., Vallier, L., Weber, A., & Dubart‐Kupperschmitt, A. (2013) · Current Gene Therapy · doi:10.2174/1566523211313020006 · Cited by 63
Endonucleases: new tools to edit the mouse genome
Wijshake, T., Baker, D. J., & van de Sluis, B. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2014.04.020 · Cited by 61
CRISPR-Cas9-Mediated In Vivo Gene Integration at the Albumin Locus Recovers Hemostasis in Neonatal and Adult Hemophilia B Mice
Wang, Q., Zhong, X., Li, Q., Su, J., Liu, Y., Mo, L., Deng, H., & Yang, Y. (2020) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2020.06.025 · Cited by 60
The in vivo fate and targeting engineering of crossover vesicle-based gene delivery system
Jiang, X., Zhang, T., & Gao, J. (2022) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2022.114324 · Cited by 61
Progress toward inducing immunologic tolerance to factor VIII
Scott, D. W., Pratt, K. P., & Miao, C. H. (2013) · Blood · doi:10.1182/blood-2013-01-478669 · Cited by 59
Gene therapy matures in the clinic
Seymour, L. W., & Thrasher, A. J. (2012) · Nature Biotechnology · doi:10.1038/nbt.2290 · Cited by 59
Hemophilia gene therapy comes of age
George, L. A. (2017) · Hematology · doi:10.1182/asheducation-2017.1.587 · Cited by 58
The gene therapy journey for hemophilia: are we there yet?
High, K. A. (2012) · Blood · doi:10.1182/blood-2012-05-423210 · Cited by 58
Self-citation
Production and Discovery of Novel Recombinant Adeno‐Associated Viral Vectors
Mueller, C., Ratner, D., Li, Z., Sena‐Esteves, M., & Gao, G. (2012) · Current Protocols in Microbiology · doi:10.1002/9780471729259.mc14d01s26 · Cited by 57
The application of genome editing in studying hearing loss
Zou, B., Mittal, R., Grati, M., Lu, Z., Shu, Y., Tao, Y., Feng, Y., Xie, D., Kong, W., Yang, S., et al. (2015) · Hearing Research · doi:10.1016/j.heares.2015.04.016 · Cited by 57
CRISPR-Cas9: a promising tool for gene editing on induced pluripotent stem cells
Kim, E. J., Kang, K. H., & Ju, J. H. (2017) · The Korean Journal of Internal Medicine · doi:10.3904/kjim.2016.198 · Cited by 58
Targeted in vivo knock-in of human alpha-1-antitrypsin cDNA using adenoviral delivery of CRISPR/Cas9
Stephens, C. J., Kashentseva, E. A., Everett, W., Kaliberova, L. N., & Curiel, D. T. (2018) · Gene Therapy · doi:10.1038/s41434-018-0003-1 · Cited by 57
Gene therapy for hemophilia
Herzog, R. W. (2015) · Frontiers in bioscience · doi:10.2741/4324 · Cited by 56
Altered intracellular localization and valosin-containing protein (p97 VCP) interaction underlie ATP7A-related distal motor neuropathy
Yi, L., Donsante, A., Kennerson, M. L., Mercer, J. F. B., Garbern, J. Y., & Kaler, S. G. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr612 · Cited by 56
Targeted Gene Addition in Human Epithelial Stem Cells by Zinc-finger Nuclease-mediated Homologous Recombination
Coluccio, A., Miselli, F., Lombardo, A., Marconi, A., Tagliazucchi, G. M., Gonçalves, M. A. F. V., Pincelli, C., Maruggi, G., Río, M. D., Naldini, L., et al. (2013) · Molecular Therapy · doi:10.1038/mt.2013.143 · Cited by 56
Genome editing for inborn errors of metabolism: advancing towards the clinic
Schneller, J. L., Lee, C. M., Bao, G., & Venditti, C. P. (2017) · BMC Medicine · doi:10.1186/s12916-017-0798-4 · Cited by 57
Advances in gene therapy for hemophilia: basis, current status, and future perspectives
Ohmori, T. (2018) · International Journal of Hematology · doi:10.1007/s12185-018-2513-4 · Cited by 60
Genetic medicines for CF: Hype versus reality
Alton, E. W. F. W., Boyd, A. C., Davies, J. C., Gill, D. R., Griesenbach, U., Harrison, P. T., Henig, N., Higgins, T., Hyde, S. C., Innes, J. A., et al. (2016) · Pediatric Pulmonology · doi:10.1002/ppul.23543 · Cited by 53
Chromatin structure in double strand break repair
Gospodinov, A. G., & Herceg, Z. (2013) · DNA repair · doi:10.1016/j.dnarep.2013.07.006 · Cited by 56
Advance trends in targeting homology-directed repair for accurate gene editing: An inclusive review of small molecules and modified CRISPR-Cas9 systems
Shams, F., Bayat, H., Mohammadian, O., Mahboudi, S., Vahidnezhad, H., Soosanabadi, M., & Rahimpour, A. (2022) · Bioimpacts · doi:10.34172/bi.2022.23871 · Cited by 53
The Scientific Quest for Lasting Youth: Prospects for Curing Aging
de Magalhães, J. P. (2014) · Rejuvenation Research · doi:10.1089/rej.2014.1580 · Cited by 54
Targeted Integration of a Super-Exon into the CFTR Locus Leads to Functional Correction of a Cystic Fibrosis Cell Line Model
Bednarski, C., Tomczak, K., Hövel, B. V., Weber, W.-M., & Cathomen, T. (2016) · PLoS ONE · doi:10.1371/journal.pone.0161072 · Cited by 56
Modeling, optimization, and comparable efficacy of T cell and hematopoietic stem cell gene editing for treating hyper‐IgM syndrome
Vavassori, V., Mercuri, E., Marcovecchio, G. E., Castiello, M. C., Schiroli, G., Albano, L., Margulies, C. M., Buquicchio, F. A., Fontana, E., Beretta, S., et al. (2021) · EMBO Molecular Medicine · doi:10.15252/emmm.202013545 · Cited by 52
Hyperactive PiggyBac Transposons for Sustained and Robust Liver-targeted Gene Therapy
Matteo, M. D., Samara-Kuko, E., Ward, N. J., Waddington, S. N., McVey, J. H., Chuah, M., & VandenDriessche, T. (2014) · Molecular Therapy · doi:10.1038/mt.2014.131 · Cited by 52
CRISPR/Cas system: An emerging technology in stem cell research
Valenti, M. T., Serena, M., Carbonare, L. D., & Zipeto, D. (2019) · World Journal of Stem Cells · doi:10.4252/wjsc.v11.i11.937 · Cited by 54
Applications of Genome Editing Technology in Animal Disease Modeling and Gene Therapy
Li, Q., Qin, Z., Wang, Q., Xu, T., Yang, Y., & He, Z. (2019) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2019.05.006 · Cited by 52
Delivery of Full-Length Factor VIII Using a piggyBac Transposon Vector to Correct a Mouse Model of Hemophilia A
Matsui, H., Fujimoto, N., Sasakawa, N., Ohinata, Y., Shima, M., Yamanaka, S., Sugimoto, M., & Hotta, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0104957 · Cited by 51
Ex vivo editing of human hematopoietic stem cells for erythroid expression of therapeutic proteins
Pavani, G., Laurent, M., Fabiano, A., Cantelli, E., Sakkal, A., Corre, G., Lenting, P. J., Concordet, J., Toueille, M., Miccio, A., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-17552-3 · Cited by 54
The gene therapy journey for hemophilia: are we there yet?
High, K. A. (2012) · PubMed · doi:10.1182/asheducation-2012.1.375 · Cited by 49
Self-citation
Personalized therapeutic strategies for patients with retinitis pigmentosa
Zheng, A., Li, Y., & Tsang, S. H. (2015) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2015.1006192 · Cited by 50
Future of rAAV Gene Therapy: Platform for RNAi, Gene Editing, and Beyond
Valdmanis, P. N., & Kay, M. A. (2017) · Human Gene Therapy · doi:10.1089/hum.2016.171 · Cited by 50
Recent trends in mucopolysaccharidosis research
Kobayashi, H. (2018) · Journal of Human Genetics · doi:10.1038/s10038-018-0534-8 · Cited by 51
Genetic correction using engineered nucleases for gene therapy applications
Li, H. L., Nakano, T., & Hotta, A. (2013) · Development Growth & Differentiation · doi:10.1111/dgd.12107 · Cited by 50
Self-citation
Gene therapy for hemophilia
Chuah, M., Evens, H., & VandenDriessche, T. (2013) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.12215 · Cited by 49
From Gene Targeting to Genome Editing: Transgenic animals applications and beyond
Rocha-Martins, M., Cavalheiro, G. R., Matos-Rodrigues, G. E., & Martins, R. A. P. (2015) · Anais da Academia Brasileira de Ciências · doi:10.1590/0001-3765201520140710 · Cited by 52
Delivering a disease-modifying treatment for Huntington's disease
Godinho, B. M. D. C., Malhotra, M., O’Driscoll, C. M., & Cryan, J. F. (2014) · Drug Discovery Today · doi:10.1016/j.drudis.2014.09.011 · Cited by 49
A universal system to select gene-modified hepatocytes in vivo
Nygaard, S. C., Barzel, A., Haft, A., Major, A. M., Finegold, M. J., Kay, M. A., & Grompe, M. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aad8166 · Cited by 47
Therapeutic homology-independent targeted integration in retina and liver
Tornabene, P., Ferla, R., Llado-Santaeularia, M., Centrulo, M., Dell’Anno, M., Esposito, F., Marrocco, E., Pone, E., Minopoli, R., Iodice, C., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-29550-8 · Cited by 48
Genetic Therapeutic Approaches for Duchenne Muscular Dystrophy
Foster, H., Popplewell, L. J., & Dickson, G. (2012) · Human Gene Therapy · doi:10.1089/hum.2012.099 · Cited by 47
Programmable Molecular Scissors: Applications of a New Tool for Genome Editing in Biotech
Saha, S. K., Saikot, F. K., Rahman, M. S., Jamal, M. A. H. M., Rahman, S. M. K., Islam, S. M. R., & Kim, K. (2018) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2018.11.016 · Cited by 48
Therapy Development by Genome Editing of Hematopoietic Stem Cells
Koniali, L., Lederer, C. W., & Kleanthous, M. (2021) · Cells · doi:10.3390/cells10061492 · Cited by 50
Hemophilia Gene Therapy: The End of the Beginning?
Wolf, D. D., Singh, K., Chuah, M., & VandenDriessche, T. (2023) · Human Gene Therapy · doi:10.1089/hum.2023.112 · Cited by 46
Chromatin structure of two genomic sites for targeted transgene integration in induced pluripotent stem cells and hematopoietic stem cells
van Rensburg, R., Beyer, I., Yao, X. Y., Wang, H., Denisenko, O. N., Li, Z. Y., Russell, D. W., Miller, D. G., Gregory, P. D., Holmes, M. C., et al. (2012) · Gene Therapy · doi:10.1038/gt.2012.25 · Cited by 46
Self-citation
Gene Repair of an Usher Syndrome Causing Mutation by Zinc-Finger Nuclease Mediated Homologous Recombination
Overlack, N., Goldmann, T., Wolfrum, U., & Nagel‐Wolfrum, K. (2012) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.12-9812 · Cited by 46
Engineering and Application of Zinc Finger Proteins and TALEs for Biomedical Research
Kim, M., & Kini, A. G. (2017) · Molecules and Cells · doi:10.14348/molcells.2017.0139 · Cited by 46
AAV vectors containing rDNA homology display increased chromosomal integration and transgene persistence
Wang, Z., Lisowski, L., Finegold, M. J., Nakai, H., Kay, M. A., & Grompe, M. (2012) · Molecular Therapy · doi:10.1038/mt.2012.157 · Cited by 44
The potential of gene therapy approaches for the treatment of hemoglobinopathies: achievements and challenges
Goodman, M., & Malik, P. (2016) · Therapeutic Advances in Hematology · doi:10.1177/2040620716653729 · Cited by 47
CCR5-edited gene therapies for HIV cure: Closing the door to viral entry
Haworth, K. G., Peterson, C. W., & Kiem, H. (2017) · Cytotherapy · doi:10.1016/j.jcyt.2017.05.013 · Cited by 46

Authors: Li, H., Haurigot, V., Doyon, Y., Li, T., Wong, S. Y., Bhagwat, A. S., Malani, N., Anguela, X. M., Sharma, R., Ivanciu, L., Murphy, S. L., Finn, J. D., Khazi, F. R., Zhou, S., Paschon, D. E., Rebar, E. J., Bushman, F. D., Gregory, P. D., Holmes, M. C., & High, K. A.
Affiliations: Children's Hospital of Philadelphia (US)
Sangamo BioSciences (United States) (US)
University of Pennsylvania (US)
Corresponding author: Holmes, Michael C.
High, Katherine A.
ORCID: Li, Hojun
Haurigot, Virginia
Doyon, Yannick
Wong, Sunnie Y.
Bhagwat, Anand S.
Malani, Nirav
Anguela, Xavier M.
Sharma, Rajiv
Finn, Jonathan D.
Rebar, Edward J.
Bushman, Frederic D.
Gregory, Philip D.
Holmes, Michael C.
High, Katherine A.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2011-06-26
Volume: 475
Issue: 7355
Pages: 217-221
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature10177
PMC: PMC3152293
OpenAlex: W2038866304
Cited by: 548
References: 29
Citations by year: 2026: 6 · 2025: 10 · 2024: 12 · 2023: 13 · 2022: 22 · 2021: 19 · 2020: 34 · 2019: 33 · 2018: 48 · 2017: 54 · 2016: 66 · 2015: 62 · 2014: 66 · 2013: 44 · 2012: 40
FWCI: 35.43
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: Howard Hughes Medical Institute
National Heart, Lung, and Blood Institute (P01HL064190, T32HL007150)
Topics: Health Sciences › Medicine › Hematology › Hemophilia Treatment and Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
Keywords: zinc finger nucleases, genome editing, hemophilia B, in vivo gene targeting, DNA double-strand breaks, homology-directed repair, gene replacement, liver regeneration, genetic disease treatment
MeSH terms: Animals, Base Sequence, Hemophilia B, Disease Models, Animal, DNA Repair, Endonucleases, Exons, Factor IX, Genetic Vectors, Hemostasis, Humans, Introns, Liver, Liver Regeneration, Mice, Inbred C57BL, Mutation, Phenotype, Genetic Therapy, Zinc Fingers, Genome, Sequence Homology, Gene Targeting, Cell Line, Tumor, Mice, DNA Breaks, Double-Stranded, HEK293 Cells

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

In vivo genome editing restores haemostasis in a mouse model of haemophilia

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks