Correspondence of Yolk Sac and Embryonic Genotypes in F0 Mouse CRISPants
Main Article Content
Abstract
CRISPR-mediated genome editing in vivo can be accompanied by prolonged stability of the Cas9 protein in mouse embryos. Then, genome edited variant alleles will be induced as long as Cas9 protein is active, and unmodified wildtype target loci are available. The corollary is that CRISPR-modified alleles that arise after the first zygotic cell division potentially could be distributed asymmetrically to the cell lineages that are specified early during morula and blastocyst development. This has practical implications for the investigation of F0 generation individuals, as cells in embryonic and extraembryonic tissues, such as the visceral yolk sac, might end up inheriting different genotypes. We here investigated the hypothetically possible scenarios by genotyping individual F0 CRISPants and their associated visceral yolk sacs in parallel. In all cases, we found that embryonic genotype was accurately reflected by yolk sac genotyping, with the two tissues indicating genetic congruence, even when the conceptus was a mosaic of cells with distinct allele configurations. Nevertheless, low abundance of a variant allele may represent a private mutation occurring only in the yolk sac, and in those rare cases, additional genotyping to determine the mutational status of the embryo proper is warranted.
Article Details
How to Cite
FUSELIER, Kayla T.B. et al.
Correspondence of Yolk Sac and Embryonic Genotypes in F0 Mouse CRISPants.
Medical Research Archives, [S.l.], v. 11, n. 6, june 2023.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/3989>. Date accessed: 23 nov. 2024.
doi: https://doi.org/10.18103/mra.v11i6.3989.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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32. Luo Y. CRISPR Gene Editing: Methods and Protocols. Humana Press. 2019 2019;
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40. Habuta M, Yasue A, Suzuki KT, et al. Fgf10-CRISPR mosaic mutants demonstrate the gene dose-related loss of the accessory lobe and decrease in the number of alveolar type 2 epithelial cells in mouse lung. PLoS One. 2020;15(10):e0240333. doi:10.1371/journal.pone.0240333
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42. Davies FC, Hope JE, McLachlan F, et al. Biallelic mutations in the gene encoding eEF1A2 cause seizures and sudden death in F0 mice. Sci Rep. Apr 5 2017;7:46019. doi:10.1038/srep46019
43. Zhong H, Chen Y, Li Y, Chen R, Mardon G. CRISPR-engineered mosaicism rapidly reveals that loss of Kcnj13 function in mice mimics human disease phenotypes. Sci Rep. Feb 10 2015;5:8366. doi:10.1038/srep08366
44. Williams M, Burdsal C, Periasamy A, Lewandoski M, Sutherland A. Mouse primitive streak forms in situ by initiation of epithelial to mesenchymal transition without migration of a cell population. Dev Dyn. Feb 2012;241(2): 270-83. doi:10.1002/dvdy.23711
45. Francou A, Anderson KV, Hadjantonakis AK. A ratchet-like apical constriction drives cell ingression during the mouse gastrulation EMT. Elife. May 10 2023;12doi:10.7554/eLife.84019
46. Ramkumar N, Anderson KV. SnapShot: mouse primitive streak. Cell. Aug 5 2011;146(3): 488-488 e2. doi:10.1016/j.cell.2011.07.028
47. Dobrovolskaïa-Zavadskaïa N. On spontaneous tail mortification in newborn mice and on the existence of a ’non-viable’ hereditary trait (factor). Soc Biol 1927; 97:116–118. Soc. Biol.1927. p. 116-118.
48. Gluecksohn-Waelsch S, Erickson RP. The T-locus of the mouse: implications for mechanisms of development. Curr Top Dev Biol. 1970;5:281-316. doi:10.1016/s0070-2153(08)60058-7
49. Herrmann BG, Labeit S, Poustka A, King TR, Lehrach H. Cloning of the T gene required in mesoderm formation in the mouse. Nature. Feb 15 1990;343(6259):617-22. doi:10.1038/343617a0
50. Wilson V, Manson L, Skarnes WC, Beddington RS. The T gene is necessary for normal mesodermal morphogenetic cell movements during gastrulation. Development. Mar 1995;121(3):877-86.
51. Teboul L, Herault Y, Wells S, Qasim W, Pavlovic G. Variability in Genome Editing Outcomes: Challenges for Research Reproducibility and Clinical Safety. Mol Ther. Jun 3 2020;28(6):1422-1431. doi:10.1016/j.ymthe.2020.03.015
52. Yamane T. Mouse Yolk Sac Hematopoiesis. Front Cell Dev Biol. 2018;6:80. doi:10.3389/fcell.2018.00080
2. Salsman J, Dellaire G. Precision genome editing in the CRISPR era. Biochem Cell Biol. Apr 2017;95(2):187-201. doi:10.1139/bcb-2016-0137
3. Sunagawa GA, Sumiyama K, Ukai-Tadenuma M, et al. Mammalian Reverse Genetics without Crossing Reveals Nr3a as a Short-Sleeper Gene. Cell Rep. Jan 26 2016;14(3):662-677. doi:10.1016/j.celrep.2015.12.052
4. Wang H, Yang H, Shivalila CS, et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell. May 9 2013;153(4):910-8. doi:10.1016/j.cell.2013.04.025
5. Fujii W, Onuma A, Sugiura K, Naito K. One-step generation of phenotype-expressing triple-knockout mice with heritable mutated alleles by the CRISPR/Cas9 system. J Reprod Dev. 2014;60(4):324-7. doi:10.1262/jrd.2013-139
6. Teboul L, Murray SA, Nolan PM. Phenotyping first-generation genome editing mutants: a new standard? Mamm Genome. Aug 2017;28(7-8):377-382. doi:10.1007/s00335-017-9711-x
7. Doench JG, Fusi N, Sullender M, et al. Optimized sgRNA design to maximize activity and minimize off-target effects of CRISPR-Cas9. Nat Biotechnol. Feb 2016;34(2):184-191. doi:10.1038/nbt.3437
8. Miyamoto S, Aoto K, Hiraide T, Nakashima M, Takabayashi S, Saitsu H. Nanopore sequencing reveals a structural alteration of mirror-image duplicated genes in a genome-editing mouse line. Congenit Anom (Kyoto). Jul 2020;60(4):120-125. doi:10.1111/cga.12364
9. Shin HY, Wang C, Lee HK, et al. CRISPR/Cas9 targeting events cause complex deletions and insertions at 17 sites in the mouse genome. Nat Commun. May 31 2017;8:15464. doi:10.1038/ncomms15464
10. Mackenzie M, Fower A, Allan AJ, Codner GF, Bunton-Stasyshyn RK, Teboul L. Genotyping Genome-Edited Founders and Subsequent Generation. Methods Mol Biol. 2023;2631:103-134. doi:10.1007/978-1-0716-2990-1_4
11. Fuselier KTB, Salbaum JM, Kappen C. Broad spectrum of CRISPR-induced edits in an embryonic lethal gene. Sci Rep. Dec 9 2021;11(1):23732. doi:10.1038/s41598-021-02627-y
12. Rossant J, Chazaud C, Yamanaka Y. Lineage allocation and asymmetries in the early mouse embryo. Philos Trans R Soc Lond B Biol Sci. Aug 29 2003;358(1436):1341-8; discussion 1349. doi:10.1098/rstb.2003.1329
13. Plusa B, Piliszek A, Frankenberg S, Artus J, Hadjantonakis AK. Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development. Sep 2008;135(18):3081-91. doi:10.1242/dev.021519
14. Papaioannou VE, Behringer RR. Early embryonic lethality in genetically engineered mice: diagnosis and phenotypic analysis. Vet Pathol. Jan 49(1):64-70. 2012. doi:0300985810395725 [pii]10.1177/0300985810395725
15. Rashbass P, Cooke LA, Herrmann BG, Beddington RS. A cell autonomous function of Brachyury in T/T embryonic stem cell chimaeras. Nature. Sep 26 1991;353(6342):348-51. doi:10.1038/353348a0
16. Taketo M, Schroeder AC, Mobraaten LE, et al. FVB/N: an inbred mouse strain preferable for transgenic analyses. Proc Natl Acad Sci U S A. Mar 15 1991;88(6):2065-9. doi:10.1073/pnas.88.6.2065
17. Hogan B, Beddington R, Costantini F, Lacy E. Manipulating the Mouse Embryo: A Laboratory Manual, second edition. Cold Spring Harbor Laboratory; 1994.
18. Jain M, Olsen HE, Paten B, Akeson M. The Oxford Nanopore MinION: delivery of nanopore sequencing to the genomics community. Genome Biol. Nov 25 2016;17(1):239. doi:10.1186/s13059-016-1103-0
19. Clement K, Rees H, Canver MC, et al. CRISPResso2 provides accurate and rapid genome editing sequence analysis. Nat Biotechnol. Mar 2019;37(3):224-226. doi:10.1038/s41587-019-0032-3
20. Schrode N, Xenopoulos P, Piliszek A, Frankenberg S, Plusa B, Hadjantonakis AK. Anatomy of a blastocyst: cell behaviors driving cell fate choice and morphogenesis in the early mouse embryo. Genesis. Apr 2013;51(4):219-33. doi:10.1002/dvg.22368
21. Bassalert C, Valverde-Estrella L, Chazaud C. Primitive Endoderm Differentiation: From Specification to Epithelialization. Curr Top Dev Biol. 2018;128:81-104. doi:10.1016/bs.ctdb.2017.12.001
22. Hara S, Kato T, Goto Y, et al. Microinjection-based generation of mutant mice with a double mutation and a 0.5 Mb deletion in their genome by the CRISPR/Cas9 system. J Reprod Dev. Oct 18 2016;62(5):531-536. doi:10.1262/jrd.2016-058
23. Kosicki M, Tomberg K, Bradley A. Repair of double-strand breaks induced by CRISPR-Cas9 leads to large deletions and complex rearrangements. Nat Biotechnol. Sep 2018;36(8):765-771. doi:10.1038/nbt.4192
24. Korablev A, Lukyanchikova V, Serova I, Battulin N. On-Target CRISPR/Cas9 Activity Can Cause Undesigned Large Deletion in Mouse Zygotes. Int J Mol Sci. May 20 2020;21(10)doi:10.3390/ijms21103604
25. Simeonov DR, Brandt AJ, Chan AY, et al. A large CRISPR-induced bystander mutation causes immune dysregulation. Commun Biol. 2019;2:70. doi:10.1038/s42003-019-0321-x
26. Park SH, Cao M, Pan Y, et al. Comprehensive analysis and accurate quantification of unintended large gene modifications induced by CRISPR-Cas9 gene editing. Sci Adv. Oct 21 2022;8(42):eabo7676. doi:10.1126/sciadv.abo7676
27. Thomas M, Burgio G, Adams DJ, Iyer V. Collateral damage and CRISPR genome editing. PLoS Genet. Mar 2019;15(3):e1007994. doi:10.1371/journal.pgen.1007994
28. Simpson BP, Yrigollen CM, Izda A, Davidson BL. Targeted long-read sequencing captures CRISPR editing and AAV integration outcomes in brain. Mol Ther. Mar 1 2023;31(3):760-773. doi:10.1016/j.ymthe.2023.01.004
29. Boroviak K, Fu B, Yang F, Doe B, Bradley A. Revealing hidden complexities of genomic rearrangements generated with Cas9. Sci Rep. Oct 9 2017;7(1):12867. doi:10.1038/s41598-017-12740-6
30. Blondal T, Gamba C, Moller Jagd L, et al. Verification of CRISPR editing and finding transgenic inserts by Xdrop indirect sequence capture followed by short- and long-read sequencing. Methods. Jul 2021;191:68-77. doi:10.1016/j.ymeth.2021.02.003
31. Montague TG, Cruz JM, Gagnon JA, Church GM, Valen E. CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing. Nucleic Acids Res. Jul 2014;42(Web Server issue):W401-7. doi:10.1093/nar/gku410
32. Luo Y. CRISPR Gene Editing: Methods and Protocols. Humana Press. 2019 2019;
33. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. Nov 2013;8(11):2281-2308. doi:10.1038/nprot.2013.143
34. Labun K, Montague TG, Krause M, Torres Cleuren YN, Tjeldnes H, Valen E. CHOPCHOP v3: expanding the CRISPR web toolbox beyond genome editing. Nucleic Acids Res. Jul 2 2019;47(W1):W171-W174. doi:10.1093/nar/gkz365
35. Saunders TL. The History of Transgenesis. Methods Mol Biol. 2020;2066:1-26. doi:10.1007/978-1-4939-9837-1_1
36. Qian J, Guan X, Xie B, et al. Multiplex epigenome editing of MECP2 to rescue Rett syndrome neurons. Sci Transl Med. Jan 18 2023;15(679):eadd4666. doi:10.1126/scitranslmed.add4666
37. Minami Y, Yuan Y, Ueda HR. High-throughput Genetically Modified Animal Experiments Achieved by Next-generation Mammalian Genetics. J Biol Rhythms. Apr 2022;37(2):135-151. doi:10.1177/07487304221075002
38. Kanai SM, Heffner C, Cox TC, et al. Auriculocondylar syndrome 2 results from the dominant-negative action of PLCB4 variants. Dis Model Mech. Apr 1 2022;15(4)doi:10.1242/dmm.049320
39. Nasseri S, Nikkho B, Parsa S, et al. Generation of Fam83h knockout mice by CRISPR/Cas9-mediated gene engineering. J Cell Biochem. Jul 2019;120(7):11033-11043. doi:10.1002/jcb.28381
40. Habuta M, Yasue A, Suzuki KT, et al. Fgf10-CRISPR mosaic mutants demonstrate the gene dose-related loss of the accessory lobe and decrease in the number of alveolar type 2 epithelial cells in mouse lung. PLoS One. 2020;15(10):e0240333. doi:10.1371/journal.pone.0240333
41. Brophy PD, Rasmussen M, Parida M, et al. A Gene Implicated in Activation of Retinoic Acid Receptor Targets Is a Novel Renal Agenesis Gene in Humans. Genetics. Sep 2017;207(1):215-228. doi:10.1534/genetics.117.1125
42. Davies FC, Hope JE, McLachlan F, et al. Biallelic mutations in the gene encoding eEF1A2 cause seizures and sudden death in F0 mice. Sci Rep. Apr 5 2017;7:46019. doi:10.1038/srep46019
43. Zhong H, Chen Y, Li Y, Chen R, Mardon G. CRISPR-engineered mosaicism rapidly reveals that loss of Kcnj13 function in mice mimics human disease phenotypes. Sci Rep. Feb 10 2015;5:8366. doi:10.1038/srep08366
44. Williams M, Burdsal C, Periasamy A, Lewandoski M, Sutherland A. Mouse primitive streak forms in situ by initiation of epithelial to mesenchymal transition without migration of a cell population. Dev Dyn. Feb 2012;241(2): 270-83. doi:10.1002/dvdy.23711
45. Francou A, Anderson KV, Hadjantonakis AK. A ratchet-like apical constriction drives cell ingression during the mouse gastrulation EMT. Elife. May 10 2023;12doi:10.7554/eLife.84019
46. Ramkumar N, Anderson KV. SnapShot: mouse primitive streak. Cell. Aug 5 2011;146(3): 488-488 e2. doi:10.1016/j.cell.2011.07.028
47. Dobrovolskaïa-Zavadskaïa N. On spontaneous tail mortification in newborn mice and on the existence of a ’non-viable’ hereditary trait (factor). Soc Biol 1927; 97:116–118. Soc. Biol.1927. p. 116-118.
48. Gluecksohn-Waelsch S, Erickson RP. The T-locus of the mouse: implications for mechanisms of development. Curr Top Dev Biol. 1970;5:281-316. doi:10.1016/s0070-2153(08)60058-7
49. Herrmann BG, Labeit S, Poustka A, King TR, Lehrach H. Cloning of the T gene required in mesoderm formation in the mouse. Nature. Feb 15 1990;343(6259):617-22. doi:10.1038/343617a0
50. Wilson V, Manson L, Skarnes WC, Beddington RS. The T gene is necessary for normal mesodermal morphogenetic cell movements during gastrulation. Development. Mar 1995;121(3):877-86.
51. Teboul L, Herault Y, Wells S, Qasim W, Pavlovic G. Variability in Genome Editing Outcomes: Challenges for Research Reproducibility and Clinical Safety. Mol Ther. Jun 3 2020;28(6):1422-1431. doi:10.1016/j.ymthe.2020.03.015
52. Yamane T. Mouse Yolk Sac Hematopoiesis. Front Cell Dev Biol. 2018;6:80. doi:10.3389/fcell.2018.00080