From engineering to editing the rat genome

Establishment in culture of pluripotential cells from mouse embryos

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Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells.

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One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering

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

The ground state of embryonic stem cell self-renewal

Ying, Q.-L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., Woodgett, J., Cohen, P., & Smith, A. (2008) · Nature · doi:10.1038/nature06968 · Cited by 3,442 · see citing works

Development of a Strain of Spontaneously Hypertensive Rats

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CRISPR/Cas, the Immune System of Bacteria and Archaea

Horvath, P., & Barrangou, R. (2010) · Science · doi:10.1126/science.1179555 · Cited by 2,471 · see citing works

A ROCK inhibitor permits survival of dissociated human embryonic stem cells

Watanabe, K., Ueno, M., Kamiya, D., Nishiyama, A., Matsumura, M., Wataya, T., Takahashi, J. B., Nishikawa, S., Nishikawa, S.-I., Muguruma, K., et al. (2007) · Nature Biotechnology · doi:10.1038/nbt1310 · Cited by 2,055 · see citing works

RNA-guided genetic silencing systems in bacteria and archaea

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One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering

Yang, H., Wang, H., Shivalila, C. S., Cheng, A. W., Shi, L., & Jaenisch, R. (2013) · Cell · doi:10.1016/j.cell.2013.08.022 · Cited by 1,596 · see citing works

A familial disorder of uric acid metabolism and central nervous system function

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A Mutation in the Vesicle-Trafficking Protein VAPB Causes Late-Onset Spinal Muscular Atrophy and Amyotrophic Lateral Sclerosis

Nishimura, A. L., Mitne‐Neto, M., da Silva, H. C. A., Richieri‐Costa, A., Middleton, S., Cascio, D., Kok, F., de Oliveira, J. R. M., Gillingwater, T. H., Webb, J., et al. (2004) · The American Journal of Human Genetics · doi:10.1086/425287 · Cited by 995 · see citing works

Knockout Rats via Embryo Microinjection of Zinc-Finger Nucleases

Geurts, A. M., Cost, G. J., Freyvert, Y., Zeitler, B., Miller, J. C., Choi, V. M., Jenkins, S. S., Wood, A. J., Cui, X., Meng, X., et al. (2009) · Science · doi:10.1126/science.1172447 · Cited by 924 · see citing works

Fulminant hypertension in transgenic rats harbouring the mouse Ren-2 gene

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Kisspeptin Activation of Gonadotropin Releasing Hormone Neurons and Regulation of KiSS-1 mRNA in the Male Rat

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Capture of Authentic Embryonic Stem Cells from Rat Blastocysts

Buehr, M. L., Meek, S. E., Blair, K., Yang, J. P., Ure, J., Silva, J., McLay, R., Hall, J., Ying, Q.-L., & Smith, A. G. (2008) · Cell · doi:10.1016/j.cell.2008.12.007 · Cited by 795 · see citing works

FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment

Kunath, T., Saba-El-Leil, M. K., Almosailleakh, M., Wray, J. P., Meloche, S., & Smith, A. G. (2007) · Development · doi:10.1242/dev.02880 · Cited by 785 · see citing works

The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent ‘+4’ cell markers

Muñoz, J., Stange, D. E., Schepers, A. G., van de Wetering, M., Koo, B., Itzkovitz, S., Volckmann, R., Kung, K. S., Köster, J., Radulescu, S., et al. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.166 · Cited by 758 · see citing works

Gene targeting in mice: functional analysis of the mammalian genome for the twenty-first century

Capecchi, M. (2005) · Nature reviews genetics · doi:10.1038/nrg1619 · Cited by 723 · see citing works

Germline Competent Embryonic Stem Cells Derived from Rat Blastocysts

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Gene targeting using zinc finger nucleases

Porteus, M. H., & Carroll, D. (2005) · Nature Biotechnology · doi:10.1038/nbt1125 · Cited by 641 · see citing works

Heritable gene targeting in the mouse and rat using a CRISPR-Cas system

Li, D., Qiu, Z., Shao, Y., Chen, Y., Guan, Y., Liu, M., Li, Y., Wang, L., Wang, L., Lu, X., et al. (2013) · Nature Biotechnology · doi:10.1038/nbt.2661 · Cited by 639 · see citing works

FATTY, A NEW MUTATION IN THE RAT

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Suppression of SHP-2 and ERK Signalling Promotes Self-Renewal of Mouse Embryonic Stem Cells

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Knockout rats generated by embryo microinjection of TALENs

Tesson, L., Usal, C., Ménoret, S., Leung, E., Niles, B. J., Remy, S., Santiago, Y., Vincent, A. I., Meng, X., Zhang, L., et al. (2011) · Nature Biotechnology · doi:10.1038/nbt.1940 · Cited by 585 · see citing works

Inhibition of glycogen synthase kinase-3 alleviates Tcf3 repression of the pluripotency network and increases embryonic stem cell resistance to differentiation

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Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat

Matsui, H., Takatsu, Y., Kumano, S., Matsumoto, H., & Ohtaki, T. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.05.185 · Cited by 520 · see citing works

Embryonic stem cells require Wnt proteins to prevent differentiation to epiblast stem cells

ten Berge, D., Kurek, D., Blauwkamp, T. A., Koole, W., Maas, A., Eroğlu, E., Siu, R. K., & Nusse, R. (2011) · Nature Cell Biology · doi:10.1038/ncb2314 · Cited by 462 · see citing works

Evolutionary parameters of the transcribed mammalian genome: An analysis of 2,820 orthologous rodent and human sequences

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Differential Regulation of Glycogen Synthase Kinase 3β by Insulin and Wnt Signaling

Ding, V. W., Chen, R., & McCormick, F. P. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m005342200 · Cited by 428 · see citing works

Molecular Pathway and Cell State Responsible for Dissociation-Induced Apoptosis in Human Pluripotent Stem Cells

Ohgushi, M., Matsumura, M., Eiraku, M., Murakami, K., Aramaki, T., Nishiyama, A., Muguruma, K., Nakano, T., Suga, H., Ueno, M., et al. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.06.018 · Cited by 423 · see citing works

Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR-Cas systems

Li, W., Teng, F., Li, T., & Zhou, Q. (2013) · Nature Biotechnology · doi:10.1038/nbt.2652 · Cited by 422 · see citing works

Precise and in situ genetic humanization of 6 Mb of mouse immunoglobulin genes

Macdonald, L. E., Karow, M. L., Stevens, S. G., Auerbach, W., Poueymirou, W. T., Yasenchak, J., Frendewey, D. A., Valenzuela, D. M., Giallourakis, C. C., Alt, F. W., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1323896111 · Cited by 390 · see citing works

Naive Pluripotent Stem Cells Derived Directly from Isolated Cells of the Human Inner Cell Mass

Guo, G., von Meyenn, F., Santos, F., Chen, Y., Reik, W., Bertone, P., Smith, A. G., & Nichols, J. (2016) · Stem Cell Reports · doi:10.1016/j.stemcr.2016.02.005 · Cited by 362 · see citing works

Transgenic rat model of Huntington's disease

von Hörsten, S., Schmitt, I., Nguyen, H. P., Holzmann, C., Schmidt, T., Walther, T., Bäder, M., Pabst, R., Kobbe, P., Krotova, J., et al. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg075 · Cited by 361 · see citing works

A protective role for protease-activated receptors in the airways

Cocks, T. M., Fong, B., Chow, J. M., Anderson, G. P., Frauman, A. G., Goldie, R. G., Henry, P. J., Carr, M., Hamilton, J. R., & Moffatt, J. D. (1999) · Nature · doi:10.1038/18223 · Cited by 357 · see citing works

ssODN-mediated knock-in with CRISPR-Cas for large genomic regions in zygotes

Yoshimi, K., Kunihiro, Y., Kaneko, T., Nagahora, H., Voigt, B., & Mashimo, T. (2016) · Nature Communications · doi:10.1038/ncomms10431 · Cited by 352 · see citing works

Targeted integration in rat and mouse embryos with zinc-finger nucleases

Cui, X., Ji, D., Fisher, D. A. C., Wu, Y., Briner, D. M., & Weinstein, E. J. (2010) · Nature Biotechnology · doi:10.1038/nbt.1731 · Cited by 312 · see citing works

Self-renewal of embryonic stem cells by a small molecule

Chen, S., Tae, J., Zhang, Q., Yao, S., Yan, F., Peters, E. C., Schöler, H. R., Schultz, P. G., & Ding, S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608156103 · Cited by 310 · see citing works

Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal

Yi, F., Pereira, L., Hoffman, J. A., Shy, B. R., Yuen, C. M., Liu, D. R., & Merrill, B. J. (2011) · Nature Cell Biology · doi:10.1038/ncb2283 · Cited by 303 · see citing works

A discrete period of FGF-induced Erk1/2 signalling is required for vertebrate neural specification

Stavridis, M. P., Lunn, J. S., Collins, B., & Storey, K. G. (2007) · Development · doi:10.1242/dev.02858 · Cited by 296 · see citing works

Germ-Line Transmission of a c- abl Mutation Produced by Targeted Gene Disruption in ES Cells

Schwartzberg, P. L., Goff, S. P., & Robertson, E. J. (1989) · Science · doi:10.1126/science.2554496 · Cited by 272 · see citing works

Impulse Control Disorders: Updated Review of Clinical Characteristics and Pharmacological Management

Schreiber, L. R. N., Odlaug, B., & Grant, J. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00001 · Cited by 271 · see citing works

Production of p53 gene knockout rats by homologous recombination in embryonic stem cells

Tong, C., Li, P., Wu, N. L., Yan, Y., & Ying, Q. (2010) · Nature · doi:10.1038/nature09368 · Cited by 267 · see citing works

Maintaining embryonic stem cell pluripotency with Wnt signaling

Sokol, S. Y. (2011) · Development · doi:10.1242/dev.066209 · Cited by 257 · see citing works

Generation of Knockout Rats with X-Linked Severe Combined Immunodeficiency (X-SCID) Using Zinc-Finger Nucleases

Mashimo, T., Takizawa, A., Voigt, B., Yoshimi, K., Hiai, H., Kuramoto, T., & Serikawa, T. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008870 · Cited by 241 · see citing works

A Novel Transgenic Rat Model with a Full Alzheimer's-Like Amyloid Pathology Displays Pre-Plaque Intracellular Amyloid-β-Associated Cognitive Impairment

León, W., Canneva, F., Partridge, V., Allard, S., Ferretti, M. T., DeWilde, A., Vercauteren, F., Atifeh, R., Ducatenzeiler, A., Klein, W. L., et al. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-1349 · Cited by 221 · see citing works

Differences in the Central Nervous System Distribution and Pharmacology of the Mouse 5-Hydroxytryptamine-6 Receptor Compared with Rat and Human Receptors Investigated by Radioligand Binding, Site-Directed Mutagenesis, and Molecular Modeling

Hirst, W. D., Abrahamsen, B., Blaney, F. E., Calver, A. R., Aloj, L., Price, G. W., & Medhurst, A. D. (2003) · Molecular Pharmacology · doi:10.1124/mol.64.6.1295 · Cited by 220 · see citing works

Production of knockout rats using ENU mutagenesis and a yeast-based screening assay

Zan, Y., Haag, J. D., Chen, K.-S., Shepel, L. A., Wigington, D., Wang, Y., Hu, R., Lopez-Guajardo, C. C., Brose, H. L., Porter, K. I., et al. (2003) · Nature Biotechnology · doi:10.1038/nbt830 · Cited by 217 · see citing works

Self renewal, expansion, and transfection of rat spermatogonial stem cells in culture

Hamra, F. K., Chapman, K. M., Nguyen, D., Williams-Stephens, A. A., Hammer, R. E., & Garbers, D. L. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508780102 · Cited by 210 · see citing works

Validated germline-competent embryonic stem cell lines from nonobese diabetic mice

Nichols, J., Jones, K. D., Phillips, J. M., Newland, S. A., Roode, M., Mansfield, W., Smith, A. G., & Cooke, A. (2009) · Nature Medicine · doi:10.1038/nm.1996 · Cited by 201 · see citing works

Generating rats with conditional alleles using CRISPR/Cas9

Ma, Y., Zhang, X., Shen, B., Lu, Y., Chen, W., Ma, J., Bai, L., Huang, X., & Zhang, L. (2013) · Cell Research · doi:10.1038/cr.2013.157 · Cited by 195 · see citing works

Concentration-Dependent Exchange of Replication Protein A on Single-Stranded DNA Revealed by Single-Molecule Imaging

Gibb, B., Ye, L. F., Gergoudis, S. C., Kwon, Y., Niu, H., Sung, P., & Greene, E. C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087922 · Cited by 189 · see citing works

Complete humanization of the mouse immunoglobulin loci enables efficient therapeutic antibody discovery

Lee, E.-C., Liang, Q., Ali, H., Bayliss, L., Beasley, A., Bloomfield-Gerdes, T., Bonoli, L., Brown, R., Campbell, J., Carpenter, A., et al. (2014) · Nature Biotechnology · doi:10.1038/nbt.2825 · Cited by 183 · see citing works

Allele-specific genome editing and correction of disease-associated phenotypes in rats using the CRISPR–Cas platform

Yoshimi, K., Kaneko, T., Voigt, B., & Mashimo, T. (2014) · Nature Communications · doi:10.1038/ncomms5240 · Cited by 177 · see citing works

Manipulating the Mouse Genome to Engineer Precise Functional Syntenic Replacements with Human Sequence

Wallace, H. A. C., Marques-Kranc, F., Richardson, M., Luna-Crespo, F., Sharpe, J. A., Hughes, J. R., Wood, W. G., Higgs, D. R., & Smith, A. J. H. (2007) · Cell · doi:10.1016/j.cell.2006.11.044 · Cited by 164 · see citing works

Rapid Loss of Oct-4 and Pluripotency in Cultured Rodent Blastocysts and Derivative Cell Lines1

Buehr, M. L., Nichols, J., Stenhouse, F. H., Mountford, P. S., Greenhalgh, C. J., Kantachuvesiri, S., Brooker, G. A., Mullins, J. J., & Smith, A. G. (2003) · Biology of Reproduction · doi:10.1095/biolreprod.102.006197 · Cited by 151 · see citing works

Transgenesis in rats: Technical aspects and models

Charreau, B. L., Tesson, L., Soulillou, J., Pourcel, C., & Anegón, I. (1996) · Transgenic Research · doi:10.1007/bf01972876 · Cited by 146 · see citing works

TALEN-mediated genome editing: prospects and perspectives

Wright, D. A., Li, T., Yang, B., & Spalding, M. H. (2014) · Biochemical Journal · doi:10.1042/bj20140295 · Cited by 134 · see citing works

Lack of Pulse and Surge Modes and Glutamatergic Stimulation of Luteinising Hormone Release in Kiss1 Knockout Rats

Uenoyama, Y., Nakamura, S., Hayakawa, Y., Ikegami, K., Watanabe, Y., Deura, C., Minabe, S., Tomikawa, J., Goto, T., Ieda, N., et al. (2015) · Journal of Neuroendocrinology · doi:10.1111/jne.12257 · Cited by 127 · see citing works

Identifying multiple causative genes at a single GWAS locusPreprint

Flister, M. J., Tsaih, S., O'Meara, C. C., Endres, B. T., Hoffman, M. J., Geurts, A. M., Dwinell, M. R., Lazar, J., Jacob, H. J., & Moreno, C. (2013) · Genome Research · doi:10.1101/gr.160283.113 · Cited by 114 · see citing works

Transgenic Modifications of the Rat Genome

Tesson, L., Cozzi, J., Ménoret, S., Remy, S., Usal, C., Fraichard, A., & Anegón, I. (2005) · Transgenic Research · doi:10.1007/s11248-005-5077-z · Cited by 110 · see citing works

Rat Genome Database (RGD): mapping disease onto the genome

Twigger, S. N. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.1.125 · Cited by 110 · see citing works

Generation of genetically modified rats from embryonic stem cells

Kawamata, M., & Ochiya, T. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009582107 · Cited by 102 · see citing works

Heritable Multiplex Genetic Engineering in Rats Using CRISPR/Cas9

Ma, Y., Shen, B., Zhang, X., Lu, Y., Chen, W., Ma, J., Huang, X., & Zhang, L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0089413 · Cited by 97 · see citing works

Large genomic fragment deletion and functional gene cassette knock-in via Cas9 protein mediated genome editing in one-cell rodent embryos

Wang, L., Shao, Y., Guan, Y., Li, L., Wu, L., Chen, F., Liu, M., Chen, H., Ma, Y., Ma, X., et al. (2015) · Scientific Reports · doi:10.1038/srep17517 · Cited by 97 · see citing works

Depdc5 knockout rat: A novel model of mTORopathy.

Marsan, E., Ishida, S., Schramm, A. E., Weckhuysen, S., Muraca, G., Lecas, S., Liang, N., Treins, C., Pende, M., Roussel, D., et al. (2016) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.02.010 · Cited by 95 · see citing works

Generation of Rag1 ‐knockout immunodeficient rats and mice using engineered meganucleases

Ménoret, S., Fontanière, S., Jantz, D., Tesson, L., Thinard, R., Remy, S., Usal, C., Ouisse, L., Fraichard, A., & Anegón, I. (2012) · The FASEB Journal · doi:10.1096/fj.12-219907 · Cited by 94 · see citing works

A simple and inexpensive method to fabricate a cannula system for intracranial injections in rats and mice

Kokare, D. M., Shelkar, G. P., Borkar, C. D., Nakhate, K. T., & Subhedar, N. K. (2011) · Journal of Pharmacological and Toxicological Methods · doi:10.1016/j.vascn.2011.08.002 · Cited by 93 · see citing works

Effect of Protease-Activated Receptor-2 Deficiency on Allergic Dermatitis in the Mouse Ear

Kawagoe, J., Takizawa, T., Matsumoto, J., Tamiya, M., Meek, S. E., Smith, A. J. H., Hunter, G. D., Plevin, R. J., Saito, N., Kanke, T., et al. (2002) · The Japanese Journal of Pharmacology · doi:10.1254/jjp.88.77 · Cited by 91 · see citing works

Gene targeting in the rat: advances and opportunities

Jacob, H. J., Lazar, J., Dwinell, M. R., Moreno, C., & Geurts, A. M. (2010) · Trends in Genetics · doi:10.1016/j.tig.2010.08.006 · Cited by 91 · see citing works

Generating knockout rats by transposon mutagenesis in spermatogonial stem cells

Izsvák, Z., Fröhlich, J., Grabundžija, I., Shirley, J. R., Powell, H. M., Chapman, K. M., Ivics, Z., & Hamra, F. K. (2010) · Nature Methods · doi:10.1038/nmeth.1461 · Cited by 90 · see citing works

Rats are the smart choice: Rationale for a renewed focus on rats in behavioral genetics

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Spontaneous activation of ovulated rat oocytes during in vitro culture

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Germline transgenesis in rabbits by pronuclear microinjection of Sleeping Beauty transposons

Ivics, Z., Hiripi, L., Hoffmann, O. I., Mátés, L., Yau, T. Y., Bashir, S., Zı́dek, V., Landa, V., Geurts, A. M., Pravenec, M., et al. (2014) · Nature Protocols · doi:10.1038/nprot.2014.009 · Cited by 81 · see citing works

Spermatogonial Culture Medium: An Effective and Efficient Nutrient Mixture for Culturing Rat Spermatogonial Stem Cells1

Wu, Z., Falciatori, I., Molyneux, L. A., Richardson, T. E., Chapman, K. M., & Hamra, F. K. (2009) · Biology of Reproduction · doi:10.1095/biolreprod.108.072645 · Cited by 81 · see citing works

Rapid and Cost-Effective Gene Targeting in Rat Embryonic Stem Cells by TALENs

Tong, C., Huang, G., Ashton, C., Wu, H., Yan, H., & Ying, Q. (2012) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2012.04.004 · Cited by 78 · see citing works

Target-selected mutagenesis of the rat

Smits, B. M. G., Mudde, J., Plasterk, R. H. A., & Cuppen, E. P. J. G. (2003) · Genomics · doi:10.1016/j.ygeno.2003.08.010 · Cited by 77 · see citing works

Whole-rat conditional gene knockout via genome editing

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An ENU-induced mutant archive for gene targeting in rats

Mashimo, T., Yanagihara, K., Tokuda, S., Voigt, B., Takizawa, A., Nakajima, R., Kato, M., Hirabayashi, M., Kuramoto, T., & Serikawa, T. (2008) · Nature Genetics · doi:10.1038/ng0508-514 · Cited by 77 · see citing works

Generation of rat mutants using a coat color-tagged Sleeping Beauty transposon system

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Generation and Characterization of Severe Combined Immunodeficiency Rats

Mashimo, T., Takizawa, A., Kobayashi, J., Kunihiro, Y., Yoshimi, K., Ishida, S., Tanabe, K., Yanagi, A., Tachibana, A., Hirose, J., et al. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.08.009 · Cited by 76 · see citing works

Superovulation of Immature Rats by Continuous Infusion of Follicle-Stimulating Hormone1

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National BioResource Project-Rat and Related Activities

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Generation of e GFP and Cre knockin rats by CRISPR /Cas9

Ma, Y., Ma, J., Zhang, X., Chen, W., Yu, L., Lu, Y., Bai, L., Shen, B., Huang, X., & Zhang, L. (2014) · FEBS Journal · doi:10.1111/febs.12935 · Cited by 71 · see citing works

Gastrointestinal functions of proteinase-activated receptors

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Robust Self-Renewal of Rat Embryonic Stem Cells Requires Fine-Tuning of Glycogen Synthase Kinase-3 Inhibition

Chen, Y., Blair, K. A., & Smith, A. G. (2013) · Stem Cell Reports · doi:10.1016/j.stemcr.2013.07.003 · Cited by 68 · see citing works

Germline transgenesis in rodents by pronuclear microinjection of Sleeping Beauty transposons

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Imaging learned fear circuitry in awake mice using fMRI

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Retake the Center Stage – New Development of Rat Genetics

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