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1. Response to correspondence on 'Reproducibility of CRISPR-Cas9 methods for generation of conditional mouse alleles: a multi-center evaluation'.

Author

Gurumurthy, CB, O'Brien, AR, Quadros, RM, Adams, J, Alcaide, P, Ayabe, S, Ballard, J, Batra, SK, Beauchamp, M-C, Becker, KA, Bernas, G, Brough, D, Carrillo-Salinas, F, Chan, W, Chen, H, Dawson, R, DeMambro, V, D'Hont, J, Dibb, K, Eudy, JD, Gan, L, Gao, J, Gonzales, A, Guntur, A, Guo, H, Harms, DW, Harrington, A, Hentges, KE, Humphreys, N, Imai, S, Ishii, H, Iwama, M, Jonasch, E, Karolak, M, Keavney, B, Khin, N-C, Konno, M, Kotani, Y, Kunihiro, Y, Lakshmanan, I, Larochelle, C, Lawrence, CB, Li, L, Lindner, V, Liu, X-D, Lopez-Castejon, G, Loudon, A, Lowe, J, Jerome-Majeweska, L, Matsusaka, T, Miura, H, Miyasaka, Y, Morpurgo, B, Motyl, K, Nabeshima, Y-I, Nakade, K, Nakashiba, T, Nakashima, K, Obata, Y, Ogiwara, S, Ouellet, M, Oxburgh, L, Piltz, S, Pinz, I, Ponnusamy, MP, Ray, D, Redder, RJ, Rosen, CJ, Ross, N, Ruhe, MT, Ryzhova, L, Salvador, AM, Alam, SS, Sedlacek, R, Sharma, K, Smith, C, Staes, K, Starrs, L, Sugiyama, F, Takahashi, S, Tanaka, T, Trafford, A, Uno, Y, Vanhoutte, L, Vanrockeghem, F, Willis, BJ, Wright, CS, Yamauchi, Y, Yi, X, Yoshimi, K, Zhang, X, Zhang, Y, Ohtsuka, M, Das, S, Garry, DJ, Hochepied, T, Thomas, P, Parker-Thornburg, J, Adamson, AD, Yoshiki, A, Schmouth, J-F, Golovko, A, Thompson, WR, Lloyd, KCK, Wood, JA, Cowan, M, Mashimo, T, Mizuno, S, Zhu, H, Kasparek, P, Liaw, L, Miano, JM, Burgio, G, Gurumurthy, CB, O'Brien, AR, Quadros, RM, Adams, J, Alcaide, P, Ayabe, S, Ballard, J, Batra, SK, Beauchamp, M-C, Becker, KA, Bernas, G, Brough, D, Carrillo-Salinas, F, Chan, W, Chen, H, Dawson, R, DeMambro, V, D'Hont, J, Dibb, K, Eudy, JD, Gan, L, Gao, J, Gonzales, A, Guntur, A, Guo, H, Harms, DW, Harrington, A, Hentges, KE, Humphreys, N, Imai, S, Ishii, H, Iwama, M, Jonasch, E, Karolak, M, Keavney, B, Khin, N-C, Konno, M, Kotani, Y, Kunihiro, Y, Lakshmanan, I, Larochelle, C, Lawrence, CB, Li, L, Lindner, V, Liu, X-D, Lopez-Castejon, G, Loudon, A, Lowe, J, Jerome-Majeweska, L, Matsusaka, T, Miura, H, Miyasaka, Y, Morpurgo, B, Motyl, K, Nabeshima, Y-I, Nakade, K, Nakashiba, T, Nakashima, K, Obata, Y, Ogiwara, S, Ouellet, M, Oxburgh, L, Piltz, S, Pinz, I, Ponnusamy, MP, Ray, D, Redder, RJ, Rosen, CJ, Ross, N, Ruhe, MT, Ryzhova, L, Salvador, AM, Alam, SS, Sedlacek, R, Sharma, K, Smith, C, Staes, K, Starrs, L, Sugiyama, F, Takahashi, S, Tanaka, T, Trafford, A, Uno, Y, Vanhoutte, L, Vanrockeghem, F, Willis, BJ, Wright, CS, Yamauchi, Y, Yi, X, Yoshimi, K, Zhang, X, Zhang, Y, Ohtsuka, M, Das, S, Garry, DJ, Hochepied, T, Thomas, P, Parker-Thornburg, J, Adamson, AD, Yoshiki, A, Schmouth, J-F, Golovko, A, Thompson, WR, Lloyd, KCK, Wood, JA, Cowan, M, Mashimo, T, Mizuno, S, Zhu, H, Kasparek, P, Liaw, L, Miano, JM, and Burgio, G

Published
2021

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

Author

Gurumurthy, CB, O'Brien, AR, Quadros, RM, Adams, J, Alcaide, P, Ayabe, S, Ballard, J, Batra, SK, Beauchamp, M-C, Becker, KA, Bernas, G, Brough, D, Carrillo-Salinas, F, Chan, W, Chen, H, Dawson, R, DeMambro, V, D'Hont, J, Dibb, KM, Eudy, JD, Gan, L, Gao, J, Gonzales, A, Guntur, AR, Guo, H, Harms, DW, Harrington, A, Hentges, KE, Humphreys, N, Imai, S, Ishii, H, Iwama, M, Jonasch, E, Karolak, M, Keavney, B, Khin, N-C, Konno, M, Kotani, Y, Kunihiro, Y, Lakshmanan, I, Larochelle, C, Lawrence, CB, Li, L, Lindner, V, Liu, X-D, Lopez-Castejon, G, Loudon, A, Lowe, J, Jerome-Majewska, LA, Matsusaka, T, Miura, H, Miyasaka, Y, Morpurgo, B, Motyl, K, Nabeshima, Y-I, Nakade, K, Nakashiba, T, Nakashima, K, Obata, Y, Ogiwara, S, Ouellet, M, Oxburgh, L, Piltz, S, Pinz, I, Ponnusamy, MP, Ray, D, Redder, RJ, Rosen, CJ, Ross, N, Ruhe, MT, Ryzhova, L, Salvador, AM, Alam, SS, Sedlacek, R, Sharma, K, Smith, C, Staes, K, Starrs, L, Sugiyama, F, Takahashi, S, Tanaka, T, Trafford, AW, Uno, Y, Vanhoutte, L, Vanrockeghem, F, Willis, BJ, Wright, CS, Yamauchi, Y, Yi, X, Yoshimi, K, Zhang, X, Zhang, Y, Ohtsuka, M, Das, S, Garry, DJ, Hochepied, T, Thomas, P, Parker-Thornburg, J, Adamson, AD, Yoshiki, A, Schmouth, J-F, Golovko, A, Thompson, WR, Lloyd, KCK, Wood, JA, Cowan, M, Mashimo, T, Mizuno, S, Zhu, H, Kasparek, P, Liaw, L, Miano, JM, Burgio, G, Gurumurthy, CB, O'Brien, AR, Quadros, RM, Adams, J, Alcaide, P, Ayabe, S, Ballard, J, Batra, SK, Beauchamp, M-C, Becker, KA, Bernas, G, Brough, D, Carrillo-Salinas, F, Chan, W, Chen, H, Dawson, R, DeMambro, V, D'Hont, J, Dibb, KM, Eudy, JD, Gan, L, Gao, J, Gonzales, A, Guntur, AR, Guo, H, Harms, DW, Harrington, A, Hentges, KE, Humphreys, N, Imai, S, Ishii, H, Iwama, M, Jonasch, E, Karolak, M, Keavney, B, Khin, N-C, Konno, M, Kotani, Y, Kunihiro, Y, Lakshmanan, I, Larochelle, C, Lawrence, CB, Li, L, Lindner, V, Liu, X-D, Lopez-Castejon, G, Loudon, A, Lowe, J, Jerome-Majewska, LA, Matsusaka, T, Miura, H, Miyasaka, Y, Morpurgo, B, Motyl, K, Nabeshima, Y-I, Nakade, K, Nakashiba, T, Nakashima, K, Obata, Y, Ogiwara, S, Ouellet, M, Oxburgh, L, Piltz, S, Pinz, I, Ponnusamy, MP, Ray, D, Redder, RJ, Rosen, CJ, Ross, N, Ruhe, MT, Ryzhova, L, Salvador, AM, Alam, SS, Sedlacek, R, Sharma, K, Smith, C, Staes, K, Starrs, L, Sugiyama, F, Takahashi, S, Tanaka, T, Trafford, AW, Uno, Y, Vanhoutte, L, Vanrockeghem, F, Willis, BJ, Wright, CS, Yamauchi, Y, Yi, X, Yoshimi, K, Zhang, X, Zhang, Y, Ohtsuka, M, Das, S, Garry, DJ, Hochepied, T, Thomas, P, Parker-Thornburg, J, Adamson, AD, Yoshiki, A, Schmouth, J-F, Golovko, A, Thompson, WR, Lloyd, KCK, Wood, JA, Cowan, M, Mashimo, T, Mizuno, S, Zhu, H, Kasparek, P, Liaw, L, Miano, JM, and Burgio, G

Abstract

BACKGROUND: CRISPR-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). RESULTS: We 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. CONCLUSION: We 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

3. Response to correspondence on "Reproducibility of CRISPR-Cas9 methods for generation of conditional mouse alleles: a multi-center evaluation".

Author

Gurumurthy CB, O'Brien AR, Quadros RM, Adams J Jr, Alcaide P, Ayabe S, Ballard J, Batra SK, Beauchamp MC, Becker KA, Bernas G, Brough D, Carrillo-Salinas F, Chan W, Chen H, Dawson R, DeMambro V, D'Hont J, Dibb K, Eudy JD, Gan L, Gao J, Gonzales A, Guntur A, Guo H, Harms DW, Harrington A, Hentges KE, Humphreys N, Imai S, Ishii H, Iwama M, Jonasch E, Karolak M, Keavney B, Khin NC, Konno M, Kotani Y, Kunihiro Y, Lakshmanan I, Larochelle C, Lawrence CB, Li L, Lindner V, Liu XD, Lopez-Castejon G, Loudon A, Lowe J, Jerome-Majeweska L, Matsusaka T, Miura H, Miyasaka Y, Morpurgo B, Motyl K, Nabeshima YI, Nakade K, Nakashiba T, Nakashima K, Obata Y, Ogiwara S, Ouellet M, Oxburgh L, Piltz S, Pinz I, Ponnusamy MP, Ray D, Redder RJ, Rosen CJ, Ross N, Ruhe MT, Ryzhova L, Salvador AM, Alam SS, Sedlacek R, Sharma K, Smith C, Staes K, Starrs L, Sugiyama F, Takahashi S, Tanaka T, Trafford A, Uno Y, Vanhoutte L, Vanrockeghem F, Willis BJ, Wright CS, Yamauchi Y, Yi X, Yoshimi K, Zhang X, Zhang Y, Ohtsuka M, Das S, Garry DJ, Hochepied T, Thomas P, Parker-Thornburg J, Adamson AD, Yoshiki A, Schmouth JF, Golovko A, Thompson WR, Lloyd KCK, Wood JA, Cowan M, Mashimo T, Mizuno S, Zhu H, Kasparek P, Liaw L, Miano JM, and Burgio G

Subjects
Alleles, Animals, Gene Editing, Mice, Reproducibility of Results, CRISPR-Associated Protein 9 metabolism, CRISPR-Cas Systems
Published
2021
Full Text
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4. Reproducibility of CRISPR-Cas9 methods for generation of conditional mouse alleles: a multi-center evaluation.

Author

Gurumurthy CB, O'Brien AR, Quadros RM, Adams J Jr, Alcaide P, Ayabe S, Ballard J, Batra SK, Beauchamp MC, Becker KA, Bernas G, Brough D, Carrillo-Salinas F, Chan W, Chen H, Dawson R, DeMambro V, D'Hont J, Dibb KM, Eudy JD, Gan L, Gao J, Gonzales A, Guntur AR, Guo H, Harms DW, Harrington A, Hentges KE, Humphreys N, Imai S, Ishii H, Iwama M, Jonasch E, Karolak M, Keavney B, Khin NC, Konno M, Kotani Y, Kunihiro Y, Lakshmanan I, Larochelle C, Lawrence CB, Li L, Lindner V, Liu XD, Lopez-Castejon G, Loudon A, Lowe J, Jerome-Majewska LA, Matsusaka T, Miura H, Miyasaka Y, Morpurgo B, Motyl K, Nabeshima YI, Nakade K, Nakashiba T, Nakashima K, Obata Y, Ogiwara S, Ouellet M, Oxburgh L, Piltz S, Pinz I, Ponnusamy MP, Ray D, Redder RJ, Rosen CJ, Ross N, Ruhe MT, Ryzhova L, Salvador AM, Alam SS, Sedlacek R, Sharma K, Smith C, Staes K, Starrs L, Sugiyama F, Takahashi S, Tanaka T, Trafford AW, Uno Y, Vanhoutte L, Vanrockeghem F, Willis BJ, Wright CS, Yamauchi Y, Yi X, Yoshimi K, Zhang X, Zhang Y, Ohtsuka M, Das S, Garry DJ, Hochepied T, Thomas P, Parker-Thornburg J, Adamson AD, Yoshiki A, Schmouth JF, Golovko A, Thompson WR, Lloyd KCK, Wood JA, Cowan M, Mashimo T, Mizuno S, Zhu H, Kasparek P, Liaw L, Miano JM, and Burgio G

Subjects
Animals, Blastocyst metabolism, Factor Analysis, Statistical, Female, Male, Methyl-CpG-Binding Protein 2 genetics, Methyl-CpG-Binding Protein 2 metabolism, Mice, Knockout, Microinjections, Regression Analysis, Reproducibility of Results, Alleles, CRISPR-Associated Protein 9 metabolism, CRISPR-Cas Systems genetics
Abstract

Background: CRISPR-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)., Results: We 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., Conclusion: We 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
Full Text
View/download PDF

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