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5. Reproducibility of CRISPR-Cas9 methods for generation of conditional mouse alleles: a multi-center evaluation

Author

Gurumurthy, Channabasavaiah B, O’Brien, Aidan R, Quadros, Rolen M, Adams, John, Alcaide, Pilar, Ayabe, Shinya, Ballard, Johnathan, Batra, Surinder K, Beauchamp, Marie-Claude, Becker, Kathleen A, Bernas, Guillaume, Brough, David, Carrillo-Salinas, Francisco, Chan, Wesley, Chen, Hanying, Dawson, Ruby, DeMambro, Victoria, D’Hont, Jinke, Dibb, Katharine M, Eudy, James D, Gan, Lin, Gao, Jing, Gonzales, Amy, Guntur, Anyonya R, Guo, Huiping, Harms, Donald W, Harrington, Anne, Hentges, Kathryn E, Humphreys, Neil, Imai, Shiho, Ishii, Hideshi, Iwama, Mizuho, Jonasch, Eric, Karolak, Michelle, Keavney, Bernard, Khin, Nay-Chi, Konno, Masamitsu, Kotani, Yuko, Kunihiro, Yayoi, Lakshmanan, Imayavaramban, Larochelle, Catherine, Lawrence, Catherine B, Li, Lin, Lindner, Volkhard, Liu, Xian-De, Lopez-Castejon, Gloria, Loudon, Andrew, Lowe, Jenna, Jerome-Majewska, Loydie A, Matsusaka, Taiji, Miura, Hiromi, Miyasaka, Yoshiki, Morpurgo, Benjamin, Motyl, Katherine, Nabeshima, Yo-ichi, Nakade, Koji, Nakashiba, Toshiaki, Nakashima, Kenichi, Obata, Yuichi, Ogiwara, Sanae, Ouellet, Mariette, Oxburgh, Leif, Piltz, Sandra, Pinz, Ilka, Ponnusamy, Moorthy P, Ray, David, Redder, Ronald J, Rosen, Clifford J, Ross, Nikki, Ruhe, Mark T, Ryzhova, Larisa, Salvador, Ane M, Alam, Sabrina Shameen, Sedlacek, Radislav, Sharma, Karan, Smith, Chad, Staes, Katrien, Starrs, Lora, Sugiyama, Fumihiro, Takahashi, Satoru, Tanaka, Tomohiro, Trafford, Andrew W, Uno, Yoshihiro, Vanhoutte, Leen, Vanrockeghem, Frederique, Willis, Brandon J, Wright, Christian S, Yamauchi, Yuko, Yi, Xin, Yoshimi, Kazuto, Zhang, Xuesong, Zhang, Yu, Ohtsuka, Masato, Das, Satyabrata, Garry, Daniel J, Hochepied, Tino, Thomas, Paul, Parker-Thornburg, Jan, Adamson, Antony D, and Yoshiki, Atsushi

Subjects
Biological Sciences, Genetics, Biotechnology, Alleles, Animals, Blastocyst, CRISPR-Associated Protein 9, CRISPR-Cas Systems, Factor Analysis, Statistical, Female, Male, Methyl-CpG-Binding Protein 2, Mice, Knockout, Microinjections, Regression Analysis, Reproducibility of Results, CRISPR-Cas9, Mouse, Transgenesis, Homology-directed repair, Conditional knockout mouse, Floxed allele, Oligonucleotide, Long single-stranded DNA, Machine learning, Reproducibility, Environmental Sciences, Information and Computing Sciences, Bioinformatics
Abstract

BackgroundCRISPR-Cas9 gene-editing technology has facilitated the generation of knockout mice, providing an alternative to cumbersome and time-consuming traditional embryonic stem cell-based methods. An earlier study reported up to 16% efficiency in generating conditional knockout (cKO or floxed) alleles by microinjection of 2 single guide RNAs (sgRNA) and 2 single-stranded oligonucleotides as donors (referred herein as "two-donor floxing" method).ResultsWe re-evaluate the two-donor method from a consortium of 20 laboratories across the world. The dataset constitutes 56 genetic loci, 17,887 zygotes, and 1718 live-born mice, of which only 15 (0.87%) mice contain cKO alleles. We subject the dataset to statistical analyses and a machine learning algorithm, which reveals that none of the factors analyzed was predictive for the success of this method. We test some of the newer methods that use one-donor DNA on 18 loci for which the two-donor approach failed to produce cKO alleles. We find that the one-donor methods are 10- to 20-fold more efficient than the two-donor approach.ConclusionWe propose that the two-donor method lacks efficiency because it relies on two simultaneous recombination events in cis, an outcome that is dwarfed by pervasive accompanying undesired editing events. The methods that use one-donor DNA are fairly efficient as they rely on only one recombination event, and the probability of correct insertion of the donor cassette without unanticipated mutational events is much higher. Therefore, one-donor methods offer higher efficiencies for the routine generation of cKO animal models.

Published
2019

8. CRISPR-mediated Bmpr2 point mutation exacerbates late pulmonary vasculopathy and reduces survival in rats with experimental pulmonary hypertension

Author

Kabwe, Jane Chanda, Sawada, Hirofumi, Mitani, Yoshihide, Oshita, Hironori, Tsuboya, Naoki, Zhang, Erquan, Maruyama, Junko, Miyasaka, Yoshiki, Ko, Hideyoshi, Oya, Kazunobu, Ito, Hiromasa, Yodoya, Noriko, Otsuki, Shoichiro, Ohashi, Hiroyuki, Okamoto, Ryuji, Dohi, Kaoru, Nishimura, Yuhei, Mashimo, Tomoji, Hirayama, Masahiro, and Maruyama, Kazuo

Published
2022
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10. Response to correspondence on “Reproducibility of CRISPR-Cas9 methods for generation of conditional mouse alleles: a multi-center evaluation”

Author

Gurumurthy, Channabasavaiah B., O’Brien, Aidan R., Quadros, Rolen M., Adams, Jr, John, Alcaide, Pilar, Ayabe, Shinya, Ballard, Johnathan, Batra, Surinder K., Beauchamp, Marie-Claude, Becker, Kathleen A., Bernas, Guillaume, Brough, David, Carrillo-Salinas, Francisco, Chan, Wesley, Chen, Hanying, Dawson, Ruby, DeMambro, Victoria, D’Hont, Jinke, Dibb, Katharine, Eudy, James D., Gan, Lin, Gao, Jing, Gonzales, Amy, Guntur, Anyonya, Guo, Huiping, Harms, Donald W., Harrington, Anne, Hentges, Kathryn E., Humphreys, Neil, Imai, Shiho, Ishii, Hideshi, Iwama, Mizuho, Jonasch, Eric, Karolak, Michelle, Keavney, Bernard, Khin, Nay-Chi, Konno, Masamitsu, Kotani, Yuko, Kunihiro, Yayoi, Lakshmanan, Imayavaramban, Larochelle, Catherine, Lawrence, Catherine B., Li, Lin, Lindner, Volkhard, Liu, Xian-De, Lopez-Castejon, Gloria, Loudon, Andrew, Lowe, Jenna, Jerome-Majeweska, Loydie, Matsusaka, Taiji, Miura, Hiromi, Miyasaka, Yoshiki, Morpurgo, Benjamin, Motyl, Katherine, Nabeshima, Yo-ichi, Nakade, Koji, Nakashiba, Toshiaki, Nakashima, Kenichi, Obata, Yuichi, Ogiwara, Sanae, Ouellet, Mariette, Oxburgh, Leif, Piltz, Sandra, Pinz, Ilka, Ponnusamy, Moorthy P., Ray, David, Redder, Ronald J., Rosen, Clifford J., Ross, Nikki, Ruhe, Mark T., Ryzhova, Larisa, Salvador, Ane M., Alam, Sabrina Shameen, Sedlacek, Radislav, Sharma, Karan, Smith, Chad, Staes, Katrien, Starrs, Lora, Sugiyama, Fumihiro, Takahashi, Satoru, Tanaka, Tomohiro, Trafford, Andrew, Uno, Yoshihiro, Vanhoutte, Leen, Vanrockeghem, Frederique, Willis, Brandon J., Wright, Christian S., Yamauchi, Yuko, Yi, Xin, Yoshimi, Kazuto, Zhang, Xuesong, Zhang, Yu, Ohtsuka, Masato, Das, Satyabrata, Garry, Daniel J., Hochepied, Tino, Thomas, Paul, Parker-Thornburg, Jan, Adamson, Antony D., Yoshiki, Atsushi, Schmouth, Jean-Francois, Golovko, Andrei, Thompson, William R., Lloyd, K. C. Kent, Wood, Joshua A., Cowan, Mitra, Mashimo, Tomoji, Mizuno, Seiya, Zhu, Hao, Kasparek, Petr, Liaw, Lucy, Miano, Joseph M., and Burgio, Gaetan

Published
2021
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11. Humanized-Aquaporin-4-Expressing Rat Created by Gene-Editing Technology and Its Use to Clarify the Pathology of Neuromyelitis Optica Spectrum Disorder.

Author

Namatame, Chihiro, Abe, Yoichiro, Miyasaka, Yoshiki, Takai, Yoshiki, Matsumoto, Yuki, Takahashi, Toshiyuki, Mashimo, Tomoji, Misu, Tatsuro, Fujihara, Kazuo, Yasui, Masato, and Aoki, Masashi

Subjects
NEUROMYELITIS optica, LABORATORY rats, MYELIN basic protein, GENOME editing, RATS, IMMUNOGLOBULIN G, MYELIN proteins
Abstract

Conventional rodent neuromyelitis optica spectrum disorder (NMOSD) models using patient-derived immunoglobulin G (IgG) are potentially affected by the differences between the human and rodent aquaporin-4 (AQP4) extracellular domains (ECDs). We hypothesized that the humanization of AQP4 ECDs would make the rodent model lesions closer to human NMOSD pathology. Humanized-AQP4-expressing (hAQP4) rats were generated using genome-editing technology, and the human AQP4-specific monoclonal antibody (mAb) or six patient-derived IgGs were introduced intraperitoneally into hAQP4 rats and wild-type Lewis (WT) rats after immunization with myelin basic protein and complete Freund's adjuvant. Human AQP4-specific mAb induced astrocyte loss lesions specifically in hAQP4 rats. The patient-derived IgGs also induced NMOSD-like tissue-destructive lesions with AQP4 loss, demyelination, axonal swelling, complement deposition, and marked neutrophil and macrophage/microglia infiltration in hAQP4 rats; however, the difference in AQP4 loss lesion size and infiltrating cells was not significant between hAQP4 and WT rats. The patient-derived IgGs bound to both human and rat AQP4 M23, suggesting their binding to the shared region of human and rat AQP4 ECDs. Anti-AQP4 titers positively correlated with AQP4 loss lesion size and neutrophil and macrophage/microglia infiltration. Considering that patient-derived IgGs vary in binding sites and affinities and some of them may not bind to rodent AQP4, our hAQP4 rat is expected to reproduce NMOSD-like pathology more accurately than WT rats. [ABSTRACT FROM AUTHOR]

Published
2024
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14. CLICK: one-step generation of conditional knockout mice

Author

Miyasaka, Yoshiki, Uno, Yoshihiro, Yoshimi, Kazuto, Kunihiro, Yayoi, Yoshimura, Takuji, Tanaka, Tomohiro, Ishikubo, Harumi, Hiraoka, Yuichi, Takemoto, Norihiko, Tanaka, Takao, Ooguchi, Yoshihiro, Skehel, Paul, Aida, Tomomi, Takeda, Junji, and Mashimo, Tomoji

Published
2018
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16. A humanised rat model of osteosarcoma reveals ultrastructural differences between bone and mineralised tumour tissue

Author

Lahr, Christoph Alexander, Landgraf, Marietta, Wagner, Ferdinand, Cipitria, Amaia, Moreno- Jimenez, Ines, Bas, Onur, Schmutz, Beat, Meinert, Christoph, Dos Santos Cavalcanti, Amanda, Mashimo, Tomoji, Miyasaka, Yoshiki, Holzapfel, Boris, Shafiee, Abbas, Mcgovern, Jacqui, Hutmacher, Dietmar, Lahr, Christoph Alexander, Landgraf, Marietta, Wagner, Ferdinand, Cipitria, Amaia, Moreno- Jimenez, Ines, Bas, Onur, Schmutz, Beat, Meinert, Christoph, Dos Santos Cavalcanti, Amanda, Mashimo, Tomoji, Miyasaka, Yoshiki, Holzapfel, Boris, Shafiee, Abbas, Mcgovern, Jacqui, and Hutmacher, Dietmar

Abstract

Current xenograft animal models fail to accurately replicate the complexity of human bone disease. To gain translatable and clinically valuable data from animal models, new in vivo models need to be developed that mimic pivotal aspects of human bone physiology as well as its diseased state. Above all, an advanced bone disease model should promote the development of new treatment strategies and facilitate the conduction of common clinical interventional procedures. Here we describe the development and characterisation of an orthotopic humanised tissue-engineered osteosarcoma (OS) model in a recently genetically engineered x-linked severe combined immunodeficient (X-SCID) rat. For the first time in a genetically modified rat, our results show the successful implementation of an orthotopic humanised tissue-engineered bone niche supporting the growth of a human OS cell line including its metastatic spread to the lung. Moreover, we studied the inter- and intraspecies differences in ultrastructural composition of bone and calcified tissue produced by the tumour, pointing to the crucial role of humanised animal models.

Published
2022

18. Additional file 1 of CRISPR-mediated Bmpr2 point mutation exacerbates late pulmonary vasculopathy and reduces survival in rats with experimental pulmonary hypertension

Author

Kabwe, Jane Chanda, Sawada, Hirofumi, Mitani, Yoshihide, Oshita, Hironori, Tsuboya, Naoki, Zhang, Erquan, Maruyama, Junko, Miyasaka, Yoshiki, Ko, Hideyoshi, Oya, Kazunobu, Ito, Hiromasa, Yodoya, Noriko, Otsuki, Shoichiro, Ohashi, Hiroyuki, Okamoto, Ryuji, Dohi, Kaoru, Nishimura, Yuhei, Mashimo, Tomoji, Hirayama, Masahiro, and Maruyama, Kazuo

Abstract

Additional file 1: Table S1. Echocardiographic findings in male rats at 7 weeks of age (baseline). Table S2. Basic data of male rats evaluated at 3 weeks after MCT or saline administration. Table S3. Basic data of female rats evaluated at 3 weeks after MCT or saline administration. Table S4. Basic data of male rats evaluated at 6 months of age. Table S5. Basic data of male rats evaluated after exposure to chronic hypoxia for 3 weeks. Table S6. Basic data of male rats evaluated at 4 weeks after MCT injection. Table S7. Basic data of male rats evaluated at 4 weeks after MCT injection and treated with tadalafil. Table S8. Basic data of male rats evaluated at 6 weeks after MCT injection and treated with tadalafil. Figure S1. Reduction of phosphorylated AKT (pAKT), a noncanonical downstream substrate proteins of BMPR2 signaling, in rats with Bmpr2 mutation (+/44insG). Figure S2. Macrophage infiltration into the lung and the representative images of muscularization of distal pulmonary artery in the monocrotaline-treated rats. Figure S3. Collagen deposition and number of vessels in the left and right ventricular myocardium after 3 weeks of monocrotaline injection. Figure S4. Pulmonary phenotype in female rats after 3 weeks of monocrotaline injection is similar between wild-type and Bmpr2 mutant rats. Figure S5. Pulmonary hemodynamics, right ventricular hypertrophy and histological assessment in male rats at 6 months of age. Figure S6. Pulmonary hemodynamics, right ventricular hypertrophy and histological assessment after 3 weeks of chronic hypoxic exposure in male rats. Figure S7. Systolic aortic pressure, right ventricular systolic pressure, hematocrit and right ventricular myocardial fibrosis at 4 weeks after monocrotaline injection in wild-type and +/44insG rats. Figure S8. Endothelin receptor A levels in lungs before and 3 and 4 weeks after monocrotaline injection. Figure S9. Expression of phosphodiesterase type 5 in lungs before, 3 and 4 weeks after monocrotaline injection. Figure S10. Tadalafil treatment improves survival of wild-type and Bmpr2 mutant rats 4 weeks after monocrotaline injection. Figure S11. Long course treatment with tadalafil from day 14 to day 42 of monocrotaline in male wild-type and +/44insG rats.

Published
2022
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19. Impact of GAD65 and/or GAD67 deficiency on perinatal development in rats

Author

Jiang, Weiru, primary, Kakizaki, Toshikazu, additional, Fujihara, Kazuyuki, additional, Miyata, Shigeo, additional, Zhang, Yue, additional, Suto, Takashi, additional, Kato, Daiki, additional, Saito, Shigeru, additional, Shibasaki, Koji, additional, Ishizaki, Yasuki, additional, Isoda, Koji, additional, Yokoo, Hideaki, additional, Obinata, Hideru, additional, Hirano, Touko, additional, Miyasaka, Yoshiki, additional, Mashimo, Tomoji, additional, and Yanagawa, Yuchio, additional

Published
2021
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20. Aberrant accumulation of TMEM43 accompanied by perturbed transmural gene expression in arrhythmogenic cardiomyopathy

Author

Shinomiya, Haruki, primary, Kato, Hisakazu, additional, Kuramoto, Yuki, additional, Watanabe, Nozomi, additional, Tsuruda, Toshihiro, additional, Arimura, Tadaaki, additional, Miyashita, Yohei, additional, Miyasaka, Yoshiki, additional, Mashimo, Tomoji, additional, Takuwa, Ayako, additional, Motooka, Daisuke, additional, Okuzaki, Daisuke, additional, Matsuoka, Ken, additional, Tsukamoto, Osamu, additional, Hakui, Hideyuki, additional, Yamada, Noriaki, additional, Lee, Jong‐Kook, additional, Kioka, Hidetaka, additional, Kitakaze, Masafumi, additional, Takashima, Seiji, additional, Sakata, Yasushi, additional, and Asano, Yoshihiro, additional

Published
2021
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23. Combi-CRISPR: combination of NHEJ and HDR provides efficient and precise plasmid-based knock-ins in mice and rats

Author

Yoshimi, Kazuto, primary, Oka, Yuichiro, additional, Miyasaka, Yoshiki, additional, Kotani, Yuko, additional, Yasumura, Misato, additional, Uno, Yoshihiro, additional, Hattori, Kosuke, additional, Tanigawa, Arisa, additional, Sato, Makoto, additional, Oya, Manami, additional, Nakamura, Kazuhiro, additional, Matsushita, Natsuki, additional, Kobayashi, Kazuto, additional, and Mashimo, Tomoji, additional

Published
2020
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26. Genetic deletion of the 67‐kDa isoform of glutamate decarboxylase alters conditioned fear behavior in rats.

Author

Fujihara, Kazuyuki, Sato, Takumi, Miyasaka, Yoshiki, Mashimo, Tomoji, and Yanagawa, Yuchio

Subjects
GLUTAMATE decarboxylase, CYCLOSERINE, LABORATORY rats, MENTAL depression, FEAR, EMOTIONS
Abstract

The GABAergic system is thought to play an important role in the control of cognition and emotion, such as fear, and is related to the pathophysiology of psychiatric disorders. For example, the expression of the 67‐kDa isoform of glutamate decarboxylase (GAD67), a GABA‐producing enzyme, is downregulated in the postmortem brains of patients with major depressive disorder and schizophrenia. However, knocking out the Gad1 gene, which encodes GAD67, is lethal in mice, and thus, the association between Gad1 and cognitive/emotional functions is unclear. We recently developed Gad1 knockout rats and found that some of them can grow into adulthood. Here, we performed fear‐conditioning tests in adult Gad1 knockout rats to assess the impact of the loss of Gad1 on fear‐related behaviors and the formation of fear memory. In a protocol assessing both cued and contextual memory, Gad1 knockout rats showed a partial antiphase pattern of freezing during training and significantly excessive freezing during the contextual test compared with wild‐type rats. However, Gad1 knockout rats did not show any synchronous increase in freezing with auditory tones in the cued test. On the other hand, in a contextual memory specialized protocol, Gad1 knockout rats exhibited comparable freezing behavior to wild‐type rats, while their fear extinction was markedly impaired. These results suggest that GABA synthesis by GAD67 has differential roles in cued and contextual fear memory. [ABSTRACT FROM AUTHOR]

Published
2021
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27. Re-Evaluating One-step Generation of Mice Carrying Conditional Alleles by CRISPR-Cas9-Mediated Genome Editing Technology

Author

Gurumurthy, Channabasavaiah, primary, Quadros, Rolen, additional, Adams, John, additional, Alcaide, Pilar, additional, Ayabe, Shinya, additional, Ballard, Johnathan, additional, Batra, Surinder K., additional, Beauchamp, Marie-Claude, additional, Becker, Kathleen A, additional, Bernas, Guillaume, additional, Brough, David, additional, Carrillo-Salinas, Francisco, additional, Dawson, Ruby, additional, DeMambro, Victoria, additional, D’Hont, Jinke, additional, Dibb, Katharine, additional, Eudy, James D., additional, Gan, Lin, additional, Gao, Jing, additional, Gonzales, Amy, additional, Guntur, Anyonya, additional, Guo, Huiping, additional, Harms, Donald W., additional, Harrington, Anne, additional, Hentges, Kathryn E., additional, Humphreys, Neil, additional, Imai, Shiho, additional, Ishii, Hideshi, additional, Iwama, Mizuho, additional, Jonasch, Eric, additional, Karolak, Michelle, additional, Keavney, Bernard, additional, Khin, Nay-Chi, additional, Konno, Masamitsu, additional, Kotani, Yuko, additional, Kunihiro, Yayoi, additional, Lakshmanan, Imayavaramban, additional, Larochelle, Catherine, additional, Lawrence, Catherine B., additional, Li, Lin, additional, Lindner, Volkhard, additional, Liu, Xian-De, additional, Lopez-Castejon, Gloria, additional, Loudon, Andrew, additional, Lowe, Jenna, additional, Jerome-Majeweska, Loydie, additional, Matsusaka, Taiji, additional, Miura, Hiromi, additional, Miyasaka, Yoshiki, additional, Morpurgo, Benjamin, additional, Motyl, Katherine, additional, Nabeshima, Yo-ichi, additional, Nakade, Koji, additional, Nakashiba, Toshiaki, additional, Nakashima, Kenichi, additional, Obata, Yuichi, additional, Ogiwara, Sanae, additional, Ouellet, Mariette, additional, Oxburgh, Leif, additional, Piltz, Sandra, additional, Pinz, Ilka, additional, Ponnusamy, Moorthy P., additional, Ray, David, additional, Redder, Ronald J., additional, Rosen, Clifford J, additional, Ross, Nikki, additional, Ruhe, Mark T., additional, Ryzhova, Larisa, additional, Salvador, Ane M., additional, Sedlacek, Radislav, additional, Sharma, Karan, additional, Smith, Chad, additional, Staes, Katrien, additional, Starrs, Lora, additional, Sugiyama, Fumihiro, additional, Takahashi, Satoru, additional, Tanaka, Tomohiro, additional, Trafford, Andrew, additional, Uno, Yoshihiro, additional, Vanhoutte, Leen, additional, Vanrockeghem, Frederique, additional, Willis, Brandon J., additional, Wright, Christian S., additional, Yamauchi, Yuko, additional, Yi, Xin, additional, Yoshimi, Kazuto, additional, Zhang, Xuesong, additional, Zhang, Yu, additional, Ohtsuka, Masato, additional, Das, Satyabrata, additional, Garry, Daniel J., additional, Hochepied, Tino, additional, Thomas, Paul, additional, Parker-Thornburg, Jan, additional, Adamson, Antony D, additional, Yoshiki, Atsushi, additional, Schmouth, Jean-Francois, additional, Golovko, Andrei, additional, Thompson, William R., additional, Lloyd, KC. Kent, additional, Wood, Joshua A., additional, Cowan, Mitra, additional, Mashimo, Tomoji, additional, Mizuno, Seiya, additional, Zhu, Hao, additional, Kasparek, Petr, additional, Liaw, Lucy, additional, Miano, Joseph M., additional, and Burgio, Gaetan, additional

Published
2018
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