CRISPR Ethics: Moral Considerations for Applications of a Powerful Tool
Open accessAbstract
With the emergence of CRISPR technology, targeted editing of a wide variety of genomes is no longer an abstract hypothetical, but occurs regularly. As application areas of CRISPR are exceeding beyond research and biomedical therapies, new and existing ethical concerns abound throughout the global community about the appropriate scope of the systems' use. Here we review fundamental ethical issues including the following: 1) the extent to which CRISPR use should be permitted; 2) access to CRISPR applications; 3) whether a regulatory framework(s) for clinical research involving human subjects might accommodate all types of human genome editing, including editing of the germline; and 4) whether international regulations governing inappropriate CRISPR utilization should be crafted and publicized. We conclude that moral decision making should evolve as the science of genomic engineering advances and hold that it would be reasonable for national and supranational legislatures to consider evidence-based regulation of certain CRISPR applications for the betterment of human health and progress.
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
Cites
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.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cited works that were retracted
Works this paper cites that were later retracted, from the retraction notices publishers deposit. Major when the notice came out before this paper was published.
Cites a retracted work: 10.1038/nmeth.4293
MajorThe cited work was retracted on 2018-03-30 (notice 10.1038/nmeth.4293), before this paper was published (2019-01). Its authors could have known.
Cited work 10.1038/nmeth.4293 · retracted 2018-03-30 · notice 10.1038/nmeth.4293 · this paper published 2019-01
“Schaefer, 2017, Unexpected mutations after CRISPR–Cas9 editing in vivo, Nat. Methods, 14, 547, 10.1038/nmeth.4293”
Cites
1 retracted
Unexpected mutations after CRISPR–Cas9 editing in vivo
Schaefer, K. A., Wu, W.-H., Colgan, D. F., Tsang, S. H., Bassuk, A. G., & Mahajan, V. B. (2017) · Nature Methods · doi:10.1038/nmeth.4293 · Cited by 328 · see citing works
RetractedA Programmable Dual-RNA–Guided DNA Endonuclease in Adaptive Bacterial Immunity
Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., & Charpentier, E. (2012) · Science · doi:10.1126/science.1225829 · Cited by 17,116 · see citing works
Multiplex Genome Engineering Using CRISPR/Cas Systems
Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W., Marraffini, L. A., et al. (2013) · Science · doi:10.1126/science.1231143 · Cited by 15,339 · see citing works
Genome engineering using the CRISPR-Cas9 system
Ran, F. A., Hsu, P. D., Wright, J., Agarwala, V., Scott, D. A., & Zhang, F. (2013) · Nature Protocols · doi:10.1038/nprot.2013.143 · Cited by 11,133 · see citing works
Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage
Komor, A. C., Kim, Y. B., Packer, M. S., Zuris, J. A., & Liu, D. R. (2016) · Nature · doi:10.1038/nature17946 · Cited by 5,437 · see citing works
Repurposing CRISPR as an RNA-Guided Platform for Sequence-Specific Control of Gene Expression
Qi, L. S., Larson, M. H., Gilbert, L. A., Doudna, J. A., Weissman, J. S., Arkin, A. P., & Lim, W. A. (2013) · Cell · doi:10.1016/j.cell.2013.02.022 · Cited by 5,016 · see citing works
CRISPR-Cas12a target binding unleashes indiscriminate single-stranded DNase activity
Chen, J. S., Ma, E., Harrington, L. B., Da Costa, M., Tian, X., Palefsky, J. M., & Doudna, J. A. (2018) · Science · doi:10.1126/science.aar6245 · Cited by 4,507 · see citing works
Programmable base editing of A•T to G•C in genomic DNA without DNA cleavage
Gaudelli, N. M., Komor, A. C., Rees, H. A., Packer, M. S., Badran, A. H., Bryson, D. I., & Liu, D. R. (2017) · Nature · doi:10.1038/nature24644 · Cited by 4,184 · see citing works
ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering
Gaj, T., Gersbach, C. A., & Barbas, C. F. (2013) · Trends in Biotechnology · doi:10.1016/j.tibtech.2013.04.004 · Cited by 3,820 · see citing works
Wang, H., Yang, H., Shivalila, C. S., Dawlaty, M. M., Cheng, A. W., Zhang, F., & Jaenisch, R. (2013) · Cell · doi:10.1016/j.cell.2013.04.025 · Cited by 3,495 · see citing works
In vivo genome editing using Staphylococcus aureus Cas9
Ran, F. A., Cong, L., Yan, W. X., Scott, D. A., Gootenberg, J. S., Kriz, A. J., Zetsche, B., Shalem, O., Wu, X., Makarova, K. S., et al. (2015) · Nature · doi:10.1038/nature14299 · Cited by 2,687 · see citing works
Multiplexed and portable nucleic acid detection platform with Cas13, Cas12a, and Csm6
Gootenberg, J. S., Abudayyeh, O. O., Kellner, M. J., Joung, J., Collins, J. J., & Zhang, F. (2018) · Science · doi:10.1126/science.aaq0179 · Cited by 2,662 · see citing works
Evolution and classification of the CRISPR–Cas systems
Makarova, K. S., Haft, D. H., Barrangou, R., Brouns, S. J. J., Charpentier, E., Horvath, P., Moineau, S., Mojica, F. J. M., Wolf, Y. I., Yakunin, A. F., et al. (2011) · Nature Reviews Microbiology · doi:10.1038/nrmicro2577 · Cited by 2,512 · see citing works
An updated evolutionary classification of CRISPR–Cas systems
Makarova, K. S., Wolf, Y. I., Alkhnbashi, O. S., Costa, F., Shah, S. A., Saunders, S. J., Barrangou, R., Brouns, S. J. J., Charpentier, E., Haft, D. H., et al. (2015) · Nature Reviews Microbiology · doi:10.1038/nrmicro3569 · Cited by 2,504 · see citing works
Rationally engineered Cas9 nucleases with improved specificity
Slaymaker, I. M., Gao, L., Zetsche, B., Scott, D. A., Yan, W. X., & Zhang, F. (2016) · Science · doi:10.1126/science.aad5227 · Cited by 2,414 · see citing works
Crystal structure of Cas9 in complex with guide RNA and target DNA
Nishimasu, H., Ran, F. A., Hsu, P. D., Konermann, S., Shehata, S. I., Dohmae, N., Ishitani, R., Zhang, F., & Nureki, O. (2014) · Cell · doi:10.1016/j.cell.2014.02.001 · Cited by 2,306 · see citing works
Cytokine Storm in a Phase 1 Trial of the Anti-CD28 Monoclonal Antibody TGN1412
Suntharalingam, G., Perry, M. R., Ward, S., Brett, S. J., Castello-Cortes, A., Brunner, M. D., & Panoskaltsis, N. (2006) · New England Journal of Medicine · doi:10.1056/nejmoa063842 · Cited by 2,164 · see citing works
RNA targeting with CRISPR–Cas13
Abudayyeh, O. O., Gootenberg, J. S., Essletzbichler, P., Han, S., Joung, J., Belanto, J. J., Verdine, V., Cox, D. B. T., Kellner, M. J., Regev, A., et al. (2017) · Nature · doi:10.1038/nature24049 · Cited by 2,093 · see citing works
Mali, P., Aach, J., Stranges, P. B., Esvelt, K. M., Moosburner, M., Kosuri, S., Yang, L., & Church, G. M. (2013) · Nature Biotechnology · doi:10.1038/nbt.2675 · Cited by 1,752 · see citing works
The CRISPR tool kit for genome editing and beyond
Adli, M. (2018) · Nature Communications · doi:10.1038/s41467-018-04252-2 · Cited by 1,642 · see citing works
Self-citationEngineered CRISPR-Cas9 nucleases with altered PAM specificities
Kleinstiver, B. P., Prew, M. S., Tsai, S. Q., Topkar, V. V., Nguyen, N. T., Zheng, Z., Gonzales, A. P. W., Li, Z., Peterson, R. T., Yeh, J.-R. J., et al. (2015) · Nature · doi:10.1038/nature14592 · Cited by 1,624 · see citing works
Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems
DiCarlo, J. E., Norville, J. E., Mali, P., Rios, X., Aach, J., & Church, G. M. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt135 · Cited by 1,566 · see citing works
Evolved Cas9 variants with broad PAM compatibility and high DNA specificity
Hu, J. H., Miller, S. M., Geurts, M. H., Tang, W., Chen, L., Sun, N., Zeina, C. M., Gao, X., Rees, H. A., Lin, Z., et al. (2018) · Nature · doi:10.1038/nature26155 · Cited by 1,552 · see citing works
Schwank, G., Koo, B.-K., Sasselli, V., Dekkers, J. F., Heo, I., Demircan, T., Sasaki, N., Boymans, S., Cuppen, E., van der Ent, C. K., et al. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2013.11.002 · Cited by 1,424 · see citing works
Diversity, classification and evolution of CRISPR-Cas systems
Koonin, E. V., Makarova, K. S., & Zhang, F. (2017) · Current Opinion in Microbiology · doi:10.1016/j.mib.2017.05.008 · Cited by 1,423 · see citing works
Dunbar, C. E., High, K. A., Joung, J. K., Kohn, D. B., Ozawa, K., & Sadelain, M. (2018) · Science · doi:10.1126/science.aan4672 · Cited by 1,410 · see citing works
McDonald, J. W., Liu, X.-Z., Qu, Y., Liu, S., Mickey, S. K., Turetsky, D. M., Gottlieb, D. I., & Choi, D. W. (1999) · Nature Medicine · doi:10.1038/70986 · Cited by 1,219 · see citing works
Björklund, L. M., Sánchez‐Pernaute, R., Chung, S., Andersson, T., CHEN, I. Y., McNaught, K. S. P., Brownell, A., Jenkins, B. G., Wahlestedt, C., Kim, K. S., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.022438099 · Cited by 1,170 · see citing works
In vivo CRISPR screening identifies Ptpn2 as a cancer immunotherapy target
Manguso, R. T., Pope, H. W., Zimmer, M. D., Brown, F. D., Yates, K. B., Miller, B. C., Collins, N. B., Bi, K., LaFleur, M. W., Juneja, V. R., et al. (2017) · Nature · doi:10.1038/nature23270 · Cited by 1,147 · see citing works
Hammond, A., Galizi, R., Kyrou, K., Simoni, A., Siniscalchi, C., Katsanos, D., Gribble, M., Baker, D. A., Marois, É., Russell, S. R. H., et al. (2015) · Nature Biotechnology · doi:10.1038/nbt.3439 · Cited by 1,142 · see citing works
Efficient genome editing in plants using a CRISPR/Cas system
Feng, Z., Zhang, B., Ding, W., Liu, X., Yang, D., Wei, P., Cao, F., Zhu, S., Zhang, F., Mao, Y., et al. (2013) · Cell Research · doi:10.1038/cr.2013.114 · Cited by 1,070 · see citing works
Diversity and evolution of class 2 CRISPR–Cas systems
Shmakov, S., Smargon, A. A., Scott, D. A., Cox, D. B. T., Pyzocha, N., Yan, W. X., Abudayyeh, O. O., Gootenberg, J. S., Makarova, K. S., Wolf, Y. I., et al. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.184 · Cited by 1,056 · see citing works
CRISPR-Based Technologies for the Manipulation of Eukaryotic Genomes
Komor, A. C., Badran, A. H., & Liu, D. R. (2016) · Cell · doi:10.1016/j.cell.2016.10.044 · Cited by 1,011 · see citing works
Haft, D. H., Selengut, J., Mongodin, E. F., & Nelson, K. E. (2005) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0010060 · Cited by 981 · see citing works
Correction of a pathogenic gene mutation in human embryos
Ma, H., Marti-Gutierrez, N., Park, S.-W., Wu, J., Lee, Y., Suzuki, K., Koski, A., Ji, D., Hayama, T., Ahmed, R., et al. (2017) · Nature · doi:10.1038/nature23305 · Cited by 969 · see citing works
Genome Engineering of Drosophila with the CRISPR RNA-Guided Cas9 Nuclease
Gratz, S. J., Cummings, A. M., Nguyen, J. N., Hamm, D. C., Donohue, L. K., Harrison, M. M., Wildonger, J., & O’Connor-Giles, K. M. (2013) · Genetics · doi:10.1534/genetics.113.152710 · Cited by 959 · see citing works
Gantz, V. M., Jasinskiene, N., Tatarenkova, O., Fazekas, A., Macias, V. M., Bier, E., & James, A. A. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1521077112 · Cited by 943 · see citing works
Gene Therapy Death Prompts Review of Adenovirus Vector
Marshall, E. (1999) · Science · doi:10.1126/science.286.5448.2244 · Cited by 918 · see citing works
Heritable genome editing in C. elegans via a CRISPR-Cas9 system
Friedland, A. E., Tzur, Y. B., Esvelt, K. M., Colaiácovo, M. P., Church, G. M., & Calarco, J. A. (2013) · Nature Methods · doi:10.1038/nmeth.2532 · Cited by 899 · see citing works
Genome-wide CRISPR Screen in a Mouse Model of Tumor Growth and Metastasis
Chen, S., Sanjana, N. E., Zheng, K., Shalem, O., Lee, K., Shi, X., Scott, D. A., Song, J. W., Pan, J. Q., Weissleder, R., et al. (2015) · Cell · doi:10.1016/j.cell.2015.02.038 · Cited by 891 · see citing works
Concerning RNA-guided gene drives for the alteration of wild populations
Esvelt, K. M., Smidler, A. L., Catteruccia, F., & Church, G. M. (2014) · eLife · doi:10.7554/elife.03401 · Cited by 857 · see citing works
Hemophilia B Gene Therapy with a High-Specific-Activity Factor IX Variant
George, L. A., Sullivan, S. K., Giermasz, A., Rasko, J. E. J., Samelson-Jones, B. J., Ducore, J., Cuker, A., Sullivan, L. M., Majumdar, S., Teitel, J., et al. (2017) · New England Journal of Medicine · doi:10.1056/nejmoa1708538 · Cited by 762 · see citing works
Svitashev, S. K., Young, J. K., Schwartz, C., Gao, H., Falco, S. C., & Cigan, A. M. (2015) · PLANT PHYSIOLOGY · doi:10.1104/pp.15.00793 · Cited by 739 · see citing works
A prudent path forward for genomic engineering and germline gene modification
Baltimore, D., Berg, P. R., Botchan, M. R., Carroll, D., Charo, R. A., Church, G. M., Corn, J. E., Daley, G. Q., Doudna, J. A., Fenner, M. W., et al. (2015) · Science · doi:10.1126/science.aab1028 · Cited by 711 · see citing works
Generation of knock-in primary human T cells using Cas9 ribonucleoproteins
Schumann, K., Lin, S., Boyer, E., Simeonov, D. R., Subramaniam, M., Gate, R. E., Haliburton, G. E., Ye, C. J., Bluestone, J. A., Doudna, J. A., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1512503112 · Cited by 702 · see citing works
Substantial contribution of extrinsic risk factors to cancer development
Wu, S., Powers, S., Zhu, W., & Hannun, Y. A. (2015) · Nature · doi:10.1038/nature16166 · Cited by 666 · see citing works
Programmable RNA recognition and cleavage by CRISPR/Cas9
O’Connell, M. R., Oakes, B. L., Sternberg, S. H., East-Seletsky, A., Kaplan, M., & Doudna, J. A. (2014) · Nature · doi:10.1038/nature13769 · Cited by 631 · see citing works
Conformational control of DNA target cleavage by CRISPR–Cas9
Sternberg, S. H., LaFrance, B., Kaplan, M., & Doudna, J. A. (2015) · Nature · doi:10.1038/nature15544 · Cited by 627 · see citing works
The mutagenic chain reaction: A method for converting heterozygous to homozygous mutations
Gantz, V. M., & Bier, E. (2015) · Science · doi:10.1126/science.aaa5945 · Cited by 589 · see citing works
New CRISPR–Cas systems from uncultivated microbes
Burstein, D. E., Harrington, L. B., Strutt, S. C., Probst, A. J., Anantharaman, K., Thomas, B. C., Doudna, J. A., & Banfield, J. F. (2016) · Nature · doi:10.1038/nature21059 · Cited by 574 · see citing works
A Critical Assessment of Vector Control for Dengue Prevention
Achee, N. L., Gould, F. L., Perkins, T. A., Reiner, R. C., Morrison, A. C., Ritchie, S. A., Gubler, D. J., Teyssou, R., & Scott, T. W. (2015) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0003655 · Cited by 465 · see citing works
Drost, J., van Boxtel, R., Blokzijl, F., Mizutani, T., Sasaki, N., Sasselli, V., de Ligt, J., Behjati, S., Grolleman, J. E., van Wezel, T., et al. (2017) · Science · doi:10.1126/science.aao3130 · Cited by 461 · see citing works
One-step generation of knockout pigs by zygote injection of CRISPR/Cas system
Hai, T., Teng, F., Guo, R., Li, W., & Zhou, Q. (2014) · Cell Research · doi:10.1038/cr.2014.11 · Cited by 458 · see citing works
In vivo target gene activation via CRISPR/Cas9-mediated trans-epigenetic modulation
Liao, H.-K., Hatanaka, F., Araoka, T., Reddy, P., Wu, M.-Z., Sui, Y., Yamauchi, T., Sakurai, M., O’Keefe, D. D., Núñez-Delicado, E., et al. (2017) · Cell · doi:10.1016/j.cell.2017.10.025 · Cited by 451 · see citing works
Klann, T. S., Black, J. B., Chellappan, M., Safi, A., Song, L., Hilton, I. B., Crawford, G. E., Reddy, T. E., & Gersbach, C. A. (2017) · Nature Biotechnology · doi:10.1038/nbt.3853 · Cited by 447 · see citing works
CRISPR gene-editing tested in a person for the first time
Cyranoski, D. (2016) · Nature · doi:10.1038/nature.2016.20988 · Cited by 442 · see citing works
CRISPR-Cas Encoding of a Digital Movie into the Genomes of a Population of Living Bacteria
Shipman, S. L., Nivala, J., Macklis, J. D., & Church, G. M. (2017) · Nature · doi:10.1038/nature23017 · Cited by 361 · see citing works
A synthetic homing endonuclease-based gene drive system in the human malaria mosquito
Windbichler, N., Menichelli, M., Papathanos, P. A., Thyme, S. B., Li, H., Ulge, U. Y., Hovde, B. T., Baker, D. A., Monnat, R. J., Burt, A., et al. (2011) · Nature · doi:10.1038/nature09937 · Cited by 360 · see citing works
CRISPR-STOP: gene silencing through base-editing-induced nonsense mutations
Kuscu, C., Parlak, M., Tufan, T., Yang, J., Szlachta, K., Wei, X., Mammadov, R., & Adli, M. (2017) · Nature Methods · doi:10.1038/nmeth.4327 · Cited by 344 · see citing works
Self-citationZischewski, J., Fischer, R., & Bortesi, L. (2017) · Biotechnology Advances · doi:10.1016/j.biotechadv.2016.12.003 · Cited by 323 · see citing works
Safeguarding CRISPR-Cas9 gene drives in yeast
DiCarlo, J. E., Chavez, A., Dietz, S., Esvelt, K. M., & Church, G. M. (2015) · Nature Biotechnology · doi:10.1038/nbt.3412 · Cited by 303 · see citing works
Precise and efficient genome editing in zebrafish using the CRISPR/Cas9 system
Irion, U., Krauß, J., & Nüsslein‐Volhard, C. (2014) · Development · doi:10.1242/dev.115584 · Cited by 292 · see citing works
Biogenesis pathways of RNA guides in archaeal and bacterial CRISPR-Cas adaptive immunity
Charpentier, E., Richter, H., John van der, O. O. S. T., & White, M. F. (2015) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuv023 · Cited by 292 · see citing works
CRISPR-Cpf1 mediates efficient homology-directed repair and temperature-controlled genome editing
Moreno-Mateos, M. A., Fernández, J. P., Rouet, R., Vejnar, C. E., Lane, M., Mis, E. K., Khokha, M. K., Doudna, J. A., & Giráldez, A. J. (2017) · Nature Communications · doi:10.1038/s41467-017-01836-2 · Cited by 279 · see citing works
CRISPR-Based Technologies for the Manipulation of Eukaryotic Genomes
Komor, A. C., Badran, A. H., & Liu, D. R. (2017) · Cell · doi:10.1016/j.cell.2017.04.005 · Cited by 276 · see citing works
Efficient targeted mutagenesis in soybean by TALENs and CRISPR/Cas9
Du, H., Zeng, X., Zhao, M., Cui, X., Wang, Q., Yang, H., Cheng, H., & Yu, D. (2015) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2015.11.005 · Cited by 267 · see citing works
Kang, X., He, W., Huang, Y., Qian, Y., Chen, Y., Gao, X., Sun, X., & Fan, Y. (2016) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-016-0710-8 · Cited by 263 · see citing works
Potential pitfalls of CRISPR /Cas9‐mediated genome editing
Peng, R., Lin, G., & Li, J. (2015) · FEBS Journal · doi:10.1111/febs.13586 · Cited by 248 · see citing works
Wu, Y., Zhou, H., Fan, X., Zhang, Y., Zhang, M., Wang, Y., Xie, Z., Bai, M., Yin, Q., Liang, D., et al. (2015) · Cell Research · doi:10.1038/cr.2014.160 · Cited by 247 · see citing works
AAV-mediated direct in vivo CRISPR screen identifies functional suppressors in glioblastoma
Chow, R. D.-W., Guzman, C. D., Wang, G., Schmidt, F., Youngblood, M. W., Ye, L., Errami, Y., Dong, M. B., Martinez, M. A. Q., Zhang, S., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4620 · Cited by 236 · see citing works
Zhang, J., Zhang, H., Botella, J. R., et al. (2017) · Journal of Integrative Plant Biology · doi:10.1111/jipb.12620 · Cited by 236 · see citing works
Methods and Applications of CRISPR-Mediated Base Editing in Eukaryotic Genomes
Hess, G. T., Tycko, J., Yao, D., & Bassik, M. C. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.09.029 · Cited by 234 · see citing works
Russell, J. J., Theriot, J. A., Sood, P., Marshall, W. F., Landweber, L. F., Fritz‐Laylin, L. K., Polka, J., Oliferenko, S., Gerbich, T. M., Gladfelter, A. S., et al. (2017) · BMC Biology · doi:10.1186/s12915-017-0391-5 · Cited by 224 · see citing works
James, S. L., Collins, F. H., Welkhoff, P. A., Emerson, C., Godfray, H. C. J., Gottlieb, M., Greenwood, B. M., Lindsay, S. W., Mbogo, C. M., Okumu, F. O., et al. (2018) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.18-0083 · Cited by 218 · see citing works
Embryology policy: Revisit the 14-day rule
Hyun, I., Wilkerson, A., & Johnston, J. (2016) · Nature · doi:10.1038/533169a · Cited by 212 · see citing works
Jelenkovic, A., Sund, R., Hur, Y.-M., Yokoyama, Y., Hjelmborg, J. V. B., Möller, S., Honda, C., Magnusson, P. K. E., Pedersen, N. L., Ooki, S., et al. (2016) · Scientific Reports · doi:10.1038/srep28496 · Cited by 202 · see citing works
Zuo, E., Cai, Y., Li, K., Yu, W., Wang, B.-A., Sun, Y., Liu, Z., Liu, J., Hu, X., Wei, W., et al. (2017) · Cell Research · doi:10.1038/cr.2017.81 · Cited by 199 · see citing works
Eckhoff, P. A., Wenger, E. A., Godfray, H. C. J., & Burt, A. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1611064114 · Cited by 191 · see citing works
A global observatory for gene editing
Jasanoff, S., & Hurlbut, J. B. (2018) · Nature · doi:10.1038/d41586-018-03270-w · Cited by 190 · see citing works
In vivo genome editing improves motor function and extends survival in a mouse model of ALS
Gaj, T., Ojala, D. S., Ekman, F. K., Byrne, L. C., Limsirichai, P., & Schaffer, D. V. (2017) · Science Advances · doi:10.1126/sciadv.aar3952 · Cited by 185 · cited 1× · see citing works
“The system offers nearly boundless potential to promote progress in combating HIV [93], hemophilia [94], cancer [95], Duchenne muscular dystrophy [96], amyotrophic lateral sclerosis [97], sickle-cell anemia [98], cystic fibrosis [99], infertility [100], and any number of novel diseases.”
BackgroundRNA-dependent RNA targeting by CRISPR-Cas9
Strutt, S. C., Torrez, R. M., Kaya, E., Negrete, O. A., & Doudna, J. A. (2018) · eLife · doi:10.7554/elife.32724 · Cited by 185 · see citing works
A comprehensive survey of the mutagenic impact of common cancer cytotoxics
Szikriszt, B., Póti, Á., Pipek, O., Krzystanek, M., Kanu, N., Molnár, J., Ribli, D., Szeltner, Z., Tusnády, G., Csabai, I., et al. (2016) · Genome biology · doi:10.1186/s13059-016-0963-7 · Cited by 179 · see citing works
U.S. attitudes on human genome editing
Scheufele, D. A., Xenos, M. A., Howell, E. L., Rose, K. M., Brossard, D., & Hardy, B. W. (2017) · Science · doi:10.1126/science.aan3708 · Cited by 174 · see citing works
Genome editing of crops: A renewed opportunity for food security
Georges, F., & Ray, H. (2017) · GM crops & food · doi:10.1080/21645698.2016.1270489 · Cited by 173 · see citing works
Macroevolutionary shifts of WntA function potentiate butterfly wing-pattern diversity
Mazo‐Vargas, A., Concha, C., Livraghi, L., Massardo, D., Wallbank, R. W. R., Zhang, L., Papador, J. D., Martinez-Najera, D., Jiggins, C. D., Kronforst, M. R., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1708149114 · Cited by 164 · see citing works
Digits and fin rays share common developmental histories
Nakamura, T., Gehrke, A. R., Lemberg, J., Szymaszek, J. F., & Shubin, N. H. (2016) · Nature · doi:10.1038/nature19322 · Cited by 162 · see citing works
Human embryonic stem cell research: ethical and legal issues
Robertson, J. A. (2001) · Nature Reviews Genetics · doi:10.1038/35047594 · Cited by 158 · see citing works
Pre-bilaterian origin of the blastoporal axial organizer
Kraus, Y., Aman, A., Technau, U., & Genikhovich, G. (2016) · Nature Communications · doi:10.1038/ncomms11694 · Cited by 143 · see citing works
Three generations, no imbeciles: eugenics, the Supreme Court, and Buck v. Bell
(2009) · Choice Reviews Online · doi:10.5860/choice.46-6480 · Cited by 140 · see citing works
Do CRISPR Germline Ethics Statements Cut It?
Brokowski, C. (2018) · The CRISPR Journal · doi:10.1089/crispr.2017.0024 · Cited by 137 · see citing works
Self-citationPromoting Cas9 degradation reduces mosaic mutations in non-human primate embryos
Tu, Z., Yang, W., Yan, S., Yin, A., Gao, J., Liu, X., Zheng, Y., Zheng, J., Li, Z., Yang, S., et al. (2017) · Scientific Reports · doi:10.1038/srep42081 · Cited by 133 · see citing works
Housden, B. E., Valvezan, A. J., Kelley, C., Sopko, R., Hu, Y., Roesel, C. L., Lin, S., Buckner, M., Tao, R., Yilmazel, B., et al. (2015) · Science Signaling · doi:10.1126/scisignal.aab3729 · Cited by 132 · see citing works
Heritable CRISPR/Cas9-Mediated Genome Editing in the Yellow Fever Mosquito, Aedes aegypti
Dong, S., Lin, J., Held, N. L., Clem, R. J., Passarelli, A. L., & Franz, A. W. E. (2015) · PLoS ONE · doi:10.1371/journal.pone.0122353 · Cited by 127 · see citing works
To Reduce the Global Burden of Human Schistosomiasis, Use ‘Old Fashioned’ Snail Control
Sokolow, S. H., Wood, C. L., Jones, I. J., Lafferty, K. D., Kuris, A. M., Hsieh, M. H., & Leo, G. A. D. (2017) · Trends in Parasitology · doi:10.1016/j.pt.2017.10.002 · Cited by 127 · see citing works
DrugTargetSeqR: a genomics- and CRISPR-Cas9–based method to analyze drug targets
Kasap, C., Elemento, O., & Kapoor, T. M. (2014) · Nature Chemical Biology · doi:10.1038/nchembio.1551 · Cited by 119 · see citing works
Wang, X., Niu, Y., Zhou, J., Yu, H., Kou, Q., Lei, A., Zhao, X., Yan, H., Cai, B., Shen, Q., et al. (2016) · Scientific Reports · doi:10.1038/srep32271 · Cited by 103 · see citing works
Chu, J., Galicia-Vázquez, G., Cencic, R., Mills, J. R., Katigbak, A., Porco, J. A. J., & Pelletier, J. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.05.005 · Cited by 100 · see citing works
CRISPR/Cas9: An RNA‐guided highly precise synthetic tool for plant genome editing
Demirci, Y., Zhang, B., & Ünver, T. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.25970 · Cited by 98 · see citing works
Gene drive inhibition by the anti-CRISPR proteins AcrIIA2 and AcrIIA4 in Saccharomyces cerevisiae
Basgall, E. M., Goetting, S. C., Goeckel, M. E., Giersch, R. M., Roggenkamp, E., Schrock, M. N., Halloran, M., & Finnigan, G. C. (2018) · Microbiology · doi:10.1099/mic.0.000635 · Cited by 95 · see citing works
Investigation of the Cause of Death in a Gene-Therapy Trial
Frank, K. M., Hogarth, D. K., Miller, J. L., Mandal, S., Mease, P. J., Samulski, R. J., Weisgerber, G. A., & Hart, J. A. L. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0801066 · Cited by 92 · see citing works
The commercialization of genome-editing technologies
Brinegar, K. N., Yetisen, A. K., Choi, S. K., Vallillo, E., Ruiz‐Esparza, G. U., Prabhakar, A. M., Khademhosseini, A., & Yun, S. H. (2017) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2016.1271768 · Cited by 92 · see citing works
Moro, D., Byrne, M. M., Kennedy, M. S., et al. (2018) · Global Ecology and Conservation · doi:10.1016/j.gecco.2017.e00363 · Cited by 91 · see citing works
Kaur, R., Sidhu, P., & Singh, S. (2016) · Journal of Pharmacology and Pharmacotherapeutics · doi:10.4103/0976-500x.189661 · Cited by 89 · see citing works
Evaluating strategies for reversing CRISPR-Cas9 gene drives
Vella, M. R., Gunning, C. E., Lloyd, A. L., & Gould, F. L. (2017) · Scientific Reports · doi:10.1038/s41598-017-10633-2 · Cited by 79 · see citing works
CRISPR-Cas Technologies and Applications in Food Bacteria
Stout, E., Klaenhammer, T. R., & Barrangou, R. (2017) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-072816-024723 · Cited by 61 · see citing works
Correction of a Disease Mutation using CRISPR/Cas9-assisted Genome Editing in Japanese Black Cattle
Ikeda, M., Matsuyama, S., Akagi, S., Ohkoshi, K., Nakamura, S., Minabe, S., Kimura, K., & Hosoe, M. (2017) · Scientific Reports · doi:10.1038/s41598-017-17968-w · Cited by 59 · see citing works
ASGCT and JSGT Joint Position Statement on Human Genomic Editing
Friedmann, T., Jonlin, E. C., King, N. M. P., Torbett, B. E., Wivel, N. A., Kaneda, Y., & Sadelain, M. (2015) · Molecular Therapy · doi:10.1038/mt.2015.118 · Cited by 58 · see citing works
Busardò, F. P., Gulino, M., Napoletano, S., Zaami, S., & Frati, P. (2014) · BioMed Research International · doi:10.1155/2014/307160 · Cited by 53 · see citing works
The Sterilization of Carrie Buck.
Sherman, R. B., Smith, J. D., & Nelson, K. (1992) · The Journal of Southern History · doi:10.2307/2210215 · Cited by 50 · see citing works
Singla, D. K., Ahmed, A., Singla, R. D., & Yan, B. (2012) · Cell Transplantation · doi:10.3727/096368911x627552 · Cited by 47 · see citing works
Compelling Reasons for Repairing Human Germlines
Church, G. M. (2017) · New England Journal of Medicine · doi:10.1056/nejmp1710370 · Cited by 47 · see citing works
Targeted genome editing in primate embryos
Guo, X., & Li, X. (2015) · Cell Research · doi:10.1038/cr.2015.64 · Cited by 43 · see citing works
Potential of gene drives with genome editing to increase genetic gain in livestock breeding programs
Gonen, S., Jenko, J., Gorjanc, G., Mileham, A. J., Whitelaw, B., & Hickey, J. M. (2017) · Genetics Selection Evolution · doi:10.1186/s12711-016-0280-3 · Cited by 43 · see citing works
Tuning CRISPR-Cas9 Gene Drives in Saccharomyces cerevisiae
Roggenkamp, E., Giersch, R. M., Schrock, M. N., Turnquist, E., Halloran, M., & Finnigan, G. C. (2018) · G3 Genes Genomes Genetics · doi:10.1534/g3.117.300557 · Cited by 43 · see citing works
Current application of CRISPR/Cas9 gene-editing technique to eradication of HIV/AIDS
Huang, Z., Tomitaka, A., Raymond, A., & Nair, M. (2017) · Gene Therapy · doi:10.1038/gt.2017.35 · Cited by 42 · see citing works
ARRIGE Arrives: Toward the Responsible Use of Genome Editing
Montoliu, L., Merchant, J., Hirsch, F., et al. (2018) · The CRISPR Journal · doi:10.1089/crispr.2018.29012.mon · Cited by 33 · see citing works
Wei, C., Wang, F., Liu, W., Zhao, W., Yang, Y., Li, K., Li, X., & Shen, J. (2017) · Molecular Medicine Reports · doi:10.3892/mmr.2017.8257 · Cited by 29 · see citing works
Wen, J., Tao, W., Hao, S., & Zu, Y. (2017) · Journal of Hematology & Oncology · doi:10.1186/s13045-017-0489-9 · Cited by 28 · see citing works
Therapeutic Applications of CRISPR/Cas for Duchenne Muscular Dystrophy
Wong, T. W. Y., & Cohn, R. D. (2017) · Current Gene Therapy · doi:10.2174/1566523217666171121165046 · Cited by 28 · see citing works
A CRISPR-Based Toolbox for Studying T Cell Signal Transduction
Chi, S., Weiss, A., & Wang, H. (2016) · BioMed Research International · doi:10.1155/2016/5052369 · Cited by 26 · see citing works
Yang, M., Zhang, L. N., Stevens, J. W., & GIBSON, G. J. (2014) · Bone · doi:10.1016/j.bone.2014.09.005 · Cited by 25 · see citing works
CRISPR/Cas9-mediated multiple single guide RNAs potently abrogate pseudorabies virus replication
Tang, Y., Liu, J.-T., Wang, T.-Y., Sun, M., Tian, Z., & Cai, X. (2017) · Archives of Virology · doi:10.1007/s00705-017-3553-4 · Cited by 25 · see citing works
The hunting of the snark: the moral status of embryos, right-to-lifers, and Third World women.
Charo, R. A. (1995) · PubMed · Cited by 23 · see citing works
Targeting Unconscionable Prescription-Drug Prices — Maryland’s Anti–Price-Gouging Law
Greene, J. A., & Padula, W. V. (2017) · New England Journal of Medicine · doi:10.1056/nejmp1704907 · Cited by 22 · see citing works
Hough, S. H., Ajetunmobi, A., Brody, L., Humphryes-Kirilov, N., & Perello, E. (2016) · Personalized Medicine · doi:10.2217/pme-2016-0068 · Cited by 21 · see citing works
Personhood Status of the Human Zygote, Embryo, Fetus
Miklavcic, J. J., & Flaman, P. (2017) · The Linacre Quarterly · doi:10.1080/00243639.2017.1299896 · Cited by 20 · see citing works
Hamrahi, V. F., Goverman, J. M., Jung, W., Wu, J. C., Fischman, A. J., Tompkins, R. G., Yu, Y. M., Fagan, S. P., & Carter, E. A. (2011) · Journal of Burn Care & Research · doi:10.1097/bcr.0b013e3182331d1c · Cited by 19 · see citing works
Key elements for designing and performing a CRISPR/Cas9-based genetic screen
Shang, W., Wang, F., Fan, G., & Wang, H. (2017) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2017.09.005 · Cited by 19 · see citing works
Jordan’s stem-cell law can guide the Middle East
Dajani, R. B. (2014) · Nature · doi:10.1038/510189a · Cited by 18 · see citing works
CRISPR-Cas9 Based Genome Engineering: Opportunities in Agri-Food-Nutrition and Healthcare
Rajendran, S. R. C. K., Yau, Y., Pandey, D., & Kumar, A., V (2015) · OMICS A Journal of Integrative Biology · doi:10.1089/omi.2015.0023 · Cited by 15 · see citing works
Cutting Eugenics Out of CRISPR-Cas9
Brokowski, C., Pollack, M., & Pollack, R. (2015) · Ethics in Biology Engineering and Medicine An International Journal · doi:10.1615/ethicsbiologyengmed.2016016260 · Cited by 14 · see citing works
Self-citationAn Efficient Method for Generation of Knockout Human Embryonic Stem Cells Using CRISPR/Cas9 System
Bohačiaková, D., Renzová, T., Fedorová, V., Barák, M., Bosakova, M. K., Hampl, A., & Čajánek, L. (2017) · Stem Cells and Development · doi:10.1089/scd.2017.0058 · Cited by 14 · see citing works
Atanes, P., Ruz‐Maldonado, I., Hawkes, R. G., Liu, B., Persaud, S. J., & Amisten, S. (2018) · Cellular Physiology and Biochemistry · doi:10.1159/000487159 · Cited by 13 · see citing works
Ethics of Cancer Gene Transfer Clinical Research
Kimmelman, J. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-2727-2_15 · Cited by 9 · see citing works
Using CRISPR‐based gene drive for agriculture pest control
Courtier‐Orgogozo, V., Morizot, B., & Boëte, C. (2017) · EMBO Reports · doi:10.15252/embr.201744822 · Cited by 8 · see citing works
Editing the human genome: balancing safety and regulation
Lancet, T. (2018) · The Lancet · doi:10.1016/s0140-6736(18)30153-3 · Cited by 8 · see citing works
Wennergren, B. (1991) · PubMed · Cited by 4 · see citing works
Interested in responsible gene editing? Join the (new) club
Enserink, M. (2018) · Science · doi:10.1126/science.aat7183 · Cited by 4 · see citing works
Killing U.S. Slowly: Curing the Epidemic Rise of Cancer Drug Prices.
White, E. K. (2017) · PubMed · Cited by 3 · see citing works
CRISPR screen: a high‐throughput approach for cancer genetic research
Lu, X., Xiang, Y., & Li, X. (2015) · Clinical Genetics · doi:10.1111/cge.12606 · Cited by 1 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- 2017, Acad. Med. Sci.
Cited by
Sorted by citations
Parrotta, E. I., Lucchino, V., Scaramuzzino, L., Scalise, S., & Cuda, G. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21124354 · Cited by 88 · see citing works
- Authors
- Brokowski, C., & Adli, M.
- Affiliations
- Yale University (US)
- University of Virginia (US)
- Corresponding author
- Adli, Mazhar
- Venue
- Journal of Molecular Biology
- Publisher
- Elsevier BV
- Published
- 2019-01
- Volume
- 431
- Issue
- 1
- Pages
- 88-101
- ISSN
- 0022-2836 (ISSN-L)
- PMC
- PMC6286228
- OpenAlex
- W2807286159
- Cited by
- 320
- References
- 140
- Citations by year
- 2026: 47 · 2025: 70 · 2024: 40 · 2023: 36 · 2022: 28 · 2021: 55 · 2020: 24 · 2019: 17 · 2018: 3
- FWCI
- 2.40
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Molecular Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health/National Cancer Institute (1R01 CA211648-01)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
- Health Sciences › Medicine › Physiology › Biomedical Ethics and Regulation
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ethics and bioethics in healthcare
- Keywords
- CRISPR, human genome editing, germline editing, clinical research ethics, international regulation, ethical decision-making, genomic engineering
- MeSH terms
- Gene Editing, Decision Making, Humans, Genome, Human, Translational Research, Biomedical, Clustered Regularly Interspaced Short Palindromic Repeats, CRISPR-Cas Systems
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