The transformational impact of site-specific DNA modifiers on biomedicine and agriculture
Kathryn Polkoff, Jorge A. Piedrahita
Abstract
The development of genetically modified livestock has been dependent on incremental technological advances such as embryo transfer, homologous recombination, and somatic cell nuclear transfer (SCNT). This development rate has increased exponentially with the advent of targeted gene modifiers such as zinc finger nucleases, TAL-effector nucleases (TALENs) and clustered regularly interspaced short palindromic repeats (CRISPR-Cas). CRISPR-Cas based systems in particular have broad applicability, and have low technical and economic barriers for their implementation. As a result, they are having, and will continue to have, a transformational impact in the field of gene editing in domestic animals. With these advances also comes the responsibility to properly apply this technology so it has a beneficial effect throughout all levels of society.
Keywords
References
Aigner B, Renner S, Kessler B, Klymiuk N, Kurome M, Wünsch A, Wolf E. 2010. Transgenic pigs as models for translational biomedical research. J Mol Med, 88:653-664.
Archer GS, Dindot S, Friend TH, Walker S, Zaunbrecher G, Lawhorn B, Piedrahita JA. 2003. Hierarchical phenotypic and epigenetic variation in cloned swine. Biol Reprod, 69:430-436.
Bevacqua RJ, Fernandez-Martín R, Savy V, Canel NG, Gismondi MI, Kues WA, Carlson DF, Fahrenkrug SC, Niemann H, Taboga OA, Ferraris S, Salamone DF. 2016. Efficient edition of the bovine PRNP prion gene in somatic cells and IVF embryos using the CRISPR/Cas9 system. Theriogenology, 86:1886-1896.e1.
Black JB, Adler AF, Wang HG, D'Ippolito AM, Hutchinson HA, Reddy TE, Pitt GS, Leong KW, Gersbach CA. 2016. Targeted epigenetic remodeling of endogenous loci by CRISPR/Cas9-based transcriptional activators directly converts fibroblasts to neuronal cells. Cell Stem Cell, 19:406-414.
Boyle EA, Andreasson JOL, Chircus LM, Sternberg SH, Wu MJ, Guegler CK4, Doudna JA, Greenleaf WJ. 2017. High-throughput biochemical profiling reveals sequence determinants of dCas9 off-target binding and unbinding. Proc Natl Acad Sci USA, 114:5461-5466.
Brown A, Woods WS, Perez-Pinera P. 2016. Multiplexed targeted genome engineering using a universal nuclease-assisted vector integration system. ACS Synth Biol, 5:582-588.
Campbell KH, McWhir J, Ritchie WA, Wilmut I. 1996. Sheep cloned by nuclear transfer from a cultured cell line. Nature, 380(6569):64-66.
Chakraborty S, Ji H, Kabadi AM, Gersbach CA, Christoforou N, Leong KW. 2014. A CRISPR/Cas9- based system for reprogramming cell lineage specification. Stem Cell Reports, 3:940-947.
Chavez A, Tuttle M, Pruitt BW, Ewen-Campen B, Chari R, Ter-Ovanesyan D, Haque SJ, Cecchi RJ, Kowal EJK, Buchthal J, Housden BE, Perrimon N, Collins JJ, Church G. 2016. Comparison of Cas9 activators in multiple species. Nat Methods, 13:563-567.
Chow RD, Chen S. 2018. Cancer CRISPR screens in vivo. Trends Cancer, 4:349-358.
Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Bogdanove AJ, Voytas DF. 2010. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics, 186:757-761.
Cibelli JB, Stice SL, Golueke PJ, Kane JJ, Jerry J, Blackwell C, Ponce de León FA, Robl JM. 1998.
Cloned transgenic calves produced from nonquiescent fetal fibroblasts. Science, 280(5367):1256-1258.
Crispo M, Mulet AP, Tesson L, Barrera N, Cuadro F, dos Santos-Neto PC, Nguyen TH, Crénéguy A, Brusselle L, Anegón I, Menchaca A. 2015. Efficient generation of myostatin knock-out sheep using CRISPR/Cas9 technology and microinjection into zygotes. PLoS One, 10(8):e0136690. doi: 10.1371 /journal.pone.0136690.
Dai Y, Vaught TD, Boone J, Chen SH, Phelps CJ, Ball S, Monahan JA, Jobst PM, McCreath KJ, Lamborn AE, Cowell-Lucero JL, Wells KD, Colman A, Polejaeva IA, Ayares DL. 2002. Targeted disruption of the alpha1,3-galactosyltransferase gene in cloned pigs. Nat Biotechnol, 20:251-255.
Frock RL, Hu J, Meyers RM, Ho Y-J, Kii E, Alt FW. 2015. Genome-wide detection of DNA double-stranded breaks induced by engineered nucleases. Nat Biotechnol, 33:179-186.
Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, Sander JD. 2013. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol, 31:822-826.
Fu Y, Sander JD, Reyon D, Cascio VM, Joung JK. 2014. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat Biotechnol, 32:279- 284.
Gaj T, Gersbach CA, Barbas CF III. 2013. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol, 31:397-405.
Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH, Bryson DI, Liu DR. 2017. Programmable base editing of A•T to G•C in genomic DNA without DNA cleavage. Nature, 551(7681):464-471.
Gemberling M, Gersbach CA. 2018. Boosting, not breaking: CRISPR activators treat disease models. Mol Ther, 26:334-336.
Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA, Torres SE, Stern-Ginossar N, Brandman O, Whitehead EH, Doudna JA, Lim WA, Weissman JS, Qi LS. 2013. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell, 154:442- 451.
Gonçalves NN, Ambrósio CE, Piedrahita JA. 2014. Stem cells and regenerative medicine in domestic and companion animals: a multispecies perspective. Reprod Domest Anim, 49:2-10.
Hai T, Teng F, Guo R, Li W, Zhou Q. 2014. One-step generation of knockout pigs by zygote injection of CRISPR/Cas system. Cell Res, 24:372-375.
Heigwer F, Kerr G, Boutros M. 2014. E-CRISP: fast CRISPR target site identification. Nat Methods, 11:122- 123.
Hilton IB, D'Ippolito AM, Vockley CM, Thakore PI, Crawford GE, Reddy TE, Gersbach CA. 2015. Epigenome editing by a CRISPR/Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat Biotechnol, 33:510-517.
Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, Agarwala V, Li Y, Fine EJ, Wu X, Shalem O, Cradick TJ, Marraffini LA, Bao G, Zhang F. 2013. DNA targeting specificity of RNAguided Cas9 nucleases. Nat Biotechnol, 31:827-832.
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNAguided DNA endonuclease in adaptive bacterial immunity. Science, 337(6096):816-821.
Kim D, Bae S, Park J, Kim E, Kim S, Yu HR, Hwang J, Kim JI, Kim JS. 2015. Digenome-seq: genome-wide profiling of CRISPR-Cas9 off-target effects in human cells. Nat Methods, 12:237-243- 1 p following 243.
Kim D, Kim J, Hur JK, Been KW, Yoon SH, Kim JS. 2016. Genome-wide analysis reveals specificities of Cpf1 endonucleases in human cells. Nat Biotechnol, 34:863-868.
Kim YB, Komor AC, Levy JM, Packer MS, Zhao KT, Liu DR. 2017. Increasing the genome-targeting scope and precision of base editing with engineered Cas9-cytidine deaminase fusions. Nat Biotechnol, 35:371-376.
Klann TS, Black JB, Chellappan M, Safi A, Song L, Hilton IB, Crawford GE, Reddy TE, Gersbach CA. 2017. CRISPR-Cas9 epigenome editing enables highthroughput screening for functional regulatory elements in the human genome. Nat Biotechnol, 35:561-568.
Kleinstiver BP, Pattanayak V, Prew MS, Tsai SQ, Nguyen NT, Zheng Z, Joung JK. 2016. High-fidelity CRISPR-Cas9 nucleases with no detectable genomewide off-target effects. Nature, 529(7587):490-495.
Koh S, Piedrahita JA. 2014. From ES-like cells to induced pluripotent stem cells: a historical perspective in domestic animals. Theriogenology, 81:103-111.
Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR. 2016. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature, 533(7603):420-424.
Konermann S, Brigham MD, Trevino AE, Joung J, Abudayyeh OO, Barcena C, Hsu PD, Habib N, Gootenberg JS, Nishimasu H, Nureki O, Zhang F. 2015. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature, 517(7536):583-588.
Kues WA, Schwinzer R, Wirth D, Verhoeyen E, Lemme E, Herrmann D, Barg-Kues B, Hauser H, Wonigeit K, Niemann H. 2006. Epigenetic silencing and tissue independent expression of a novel tetracycline inducible system in double-transgenic pigs. FASEB J, 20:1200-1202.
Kuroiwa Y, Kasinathan P, Matsushita H, Sathiyaselan J, Sullivan EJ, Kakitani M, Tomizuka K, Ishida I, Robl JM. 2004. Sequential targeting of the genes encoding immunoglobulin-mu and prion protein in cattle. Nat Genet, 36:775-780.
Kwon DY, Zhao YT, Lamonica JM, Zhou Z. 2017. Locus-specific histone deacetylation using a synthetic CRISPR-Cas9-based HDAC. Nat Commun, 8:15315. doi: 10.1038/ncomms15315.
Le Provost F, Lillico S, Passet B, Young R, Whitelaw B, Vilotte J-L. 2010. Zinc finger nuclease technology heralds a new era in mammalian transgenesis. Trends Biotechnol, 28(3):134-141.
Li X, Wang Y, Liu Y, Yang B, Wang X, Wei J, Lu Z, Zhang Y, Wu J, Huang X, Yang L, Chen J. 2018. Base editing with a Cpf1-cytidine deaminase fusion. Nat Biotechnol, 36:324-327.
Liao HK, Hatanaka F, Araoka T, Reddy P, Wu MZ, Sui Y, Yamauchi T, Sakurai M, O'Keefe DD, NúñezDelicado E, Guillen P, Campistol JM, Wu CJ, Lu LF, Esteban CR, Izpisua Belmonte JC. 2017. In vivo target gene activation via CRISPR/Cas9-mediated transepigenetic modulation. Cell, 171:1495-1507. e15.
Maruyama T, Dougan SK, Truttmann MC, Bilate AM, Ingram JR, Ploegh HL. 2015. Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining. Nat Biotechnol, 33:538-542.
McCreath KJ, Howcroft J, Campbell KH, Colman A, Schnieke AE, Kind AJ. 2000. Production of genetargeted sheep by nuclear transfer from cultured somatic cells. Nature, 405(6790):1066-1069.
Ng HH, Bird A. 1999. DNA methylation and chromatin modification. Curr Opin Genet Dev, 9:158-163.
Niu Y, Zhao X, Zhou J, Li Y, Huang Y, Cai B, Liu Y, Ding Q, Zhou S, Zhao J, Zhou G, Ma B, Huang X, Wang X, Chen Y. 2018. Efficient generation of goats with defined point mutation (I397V) in GDF9 through CRISPR/Cas9. Reprod Fertil Dev, 30:307-312.
Nowak-Imialek M, Kues WA, Petersen B, LucasHahn A, Herrmann D, Haridoss S, Oropeza M, Lemme E, Schöler HR, Carnwath JW, Niemann H. 2010. Oct4-enhanced green fluorescent protein transgenic pigs: a new large animal model for reprogramming studies. Stem Cells Dev, 20:1563-1575.
Park KE, Powell A, Sandmaier SE, Kim CM, Mileham A, Donovan DM, Telugu BP. 2017. Targeted gene knock-in by CRISPR/Cas ribonucleoproteins in porcine zygotes. Sci Rep, 7:42458. doi: 10.1038/srep42458.
Perez-Pinera P, Kocak DD, Vockley CM, Adler AF, Kabadi AM, Polstein LR, Thakore PI, Glass KA, Ousterout DG, Leong KW, Guilak F, Crawford GE, Reddy TE, Gersbach CA. 2013. RNA-guided gene activation by CRISPR-Cas9-based transcription factors. Nat Methods, 10:973-976.
Piedrahita JA, Zhang SH, Hagaman JR, Oliver PM, Maeda N. 1992. Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. Proc Natl Acad Sci USA, 89:4471-4475.
Piedrahita JA, Olby N. 2011. Perspectives on transgenic livestock in agriculture and biomedicine: an update. Reprod Fertil Dev, 23:56-63.
Prather RS, Shen M, Dai Y. 2008. Genetically modified pigs for medicine and agriculture. Biotechnol Genet Eng Rev, 25:245-266.
Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, Lim WA. 2013. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell, 152:1173-1183.
Ran FA, Cong L, Yan WX, Scott DA, Gootenberg JS, Kriz AJ, Zetsche B, Shalem O, Wu X, Makarova KS, Koonin EV, Sharp PA, Zhang F. 2015. In vivo genome editing using Staphylococcus aureus Cas9. Nature, 520(7546):186-191.
Sander JD, Joung JK. 2014. CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotechnol, 32:347-355.
Schnieke AE, Kind AJ, Ritchie WA, Mycock K, Scott AR, Ritchie M, Wilmut I, Colman A, Campbell KH. 1997. Human factor IX transgenic sheep produced by transfer of nuclei from transfected fetal fibroblasts. Science, 278(5346):2130-2133.
Shen B, Zhang W, Zhang J, Zhou J, Wang J, Chen L, Wang L, Hodgkins A, Iyer V, Huang X, Skarnes WC. 2014. Efficient genome modification by CRISPRCas9 nickase with minimal off-target effects. Nat Methods, 11:399-402.
Shimatani Z, Kashojiya S, Takayama M, Terada R, Arazoe T, Ishii H, Teramura H, Yamamoto T, Komatsu H, Miura K, Ezura H, Nishida K, Ariizumi T, Kondo A. 2017. Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat Biotechnol, 35:441-443.
Smithies O, Koralewski MA, Song KY, Kucherlapati RS. 1984. Homologous recombination with DNA introduced into mammalian cells. Cold Spring Harb Symp Quant Biol, 49:161-170.
Smithies O. 2001. Forty years with homologous recombination. Nat Med, 7:1083-1086.
Smithies O. 2008. Turning pages (Nobel lecture). Chembiochem, 9:1342-1359.
Suzuki K, Tsunekawa Y, Hernandez-Benitez R, Wu J, Zhu J, Kim EJ, Hatanaka F, Yamamoto M, Araoka T, Li Z, Kurita M, Hishida T, Li M, Aizawa E, Guo S, Chen S, Goebl A, Soligalla RD, Qu J, Jiang T, Fu X, Jafari M, Esteban CR, Berggren WT, Lajara J, Nuñez-Delicado E, Guillen P, Campistol JM, Matsuzaki F, Liu GH, Magistretti P, Zhang K, Callaway EM, Zhang K, Belmonte JC. 2016. In vivo genome editing via CRISPR/Cas9 mediated homologyindependent targeted integration. Nature, 540(7631):144-149.
Tsai SQ, Zheng Z, Nguyen NT, Liebers M, Topkar VV, Thapar V, Wyvekens N, Khayter C, Iafrate AJ, Le LP, Aryee MJ, Joung JK. 2015. GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nat Biotechnol, 33:187-197.
Tsai SQ, Nguyen NT, Malagon-Lopez J, Topkar VV, Aryee MJ, Joung JK. 2017. CIRCLE-seq: a highly sensitive in vitro screen for genome-wide CRISPR-Cas9 nuclease off-targets. Nat Methods, 14:607-614.
Vazquez JC, Nogues C, Rucker EB, Piedrahita JA. 1998. Factors affecting the efficiency of introducing precise genetic changes in ES cells by homologous recombination: tag-and-exchange versus the Cre-loxp system. Transgenic Res, 7:181-193.
Vojta A, Dobrinić P, Tadić V, Bočkor L, Korać P, Julg B, Klasić M, Zoldoš V. 2016. Repurposing the CRISPR-Cas9 system for targeted DNA methylation. Nucleic Acids Res, 44:5615-5628.
Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, Jaenisch R. 2013. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell, 153:910-918.
Wang X, Yu H, Lei A, Zhou J, Zeng W, Zhu H, Dong Z, Niu Y, Shi B, Cai B, Liu J, Huang S, Yan H, Zhao X, Zhou G, He X, Chen X, Yang Y, Jiang Y, Shi L, Tian X, Wang Y, Ma B, Huang X, Qu L, Chen Y. 2015. Generation of gene-modified goats targeting MSTN and FGF5 via zygote injection of CRISPR/Cas9 system. Sci Rep, 5:13878.
Yang H, Wang H, Shivalila CS, Cheng AW, Shi L, Jaenisch R. 2013. One-step generation of mice carrying reporter and conditional alleles by CRISPR/Casmediated genome engineering. Cell, 154:1370-1379.
Yao X, Wang X, Hu X, Liu Z, Liu J, Zhou H, Shen X, Wei Y, Huang Z, Ying W, Wang Y, Nie YH, Zhang CC, Li S, Cheng L, Wang Q, Wu Y, Huang P, Sun Q, Shi L, Yang H. 2017. Homology-mediated end joining-based targeted integration using CRISPR/Cas9. Cell Res, 27:801-814.
Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS, Essletzbichler P, Volz SE, Joung J, van der Oost J, Regev A, Koonin EV, Zhang F. 2015. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell, 163:759-771.
Zhou H, Liu J, Zhou C, Gao N, Rao Z, Li H, Hu X, Li C, Yao X, Shen X, Sun Y, Wei Y, Liu F, Ying W, Zhang J, Tang C, Zhang X, Xu H, Shi L, Cheng L, Huang P, Yang H. 2018. In vivo simultaneous transcriptional activation of multiple genes in the brain using CRISPR-dCas9- activator transgenic mice. Nat Neurosci, 21: 440-446.
Facebook
Google+
Twitter
LinkedIn
Mendeley
StumbleUpon
CiteULike
Reddit
Email