Targeted Genome Editing by Recombinant Adeno-Associated Virus (rAAV) Vectors for Generating Genetically Modified Pigs

Journal of Genetics and Genomics

Volumn 39, Issue 6, 2012, Pages 269-274

  Luo, Yonglun ^a   Kofod Olsen, Emil ^a   Christensen, Rikke ^a   Sørensen, Charlotte Brandt ^a   Bolund, Lars ^a,b  

^a AARHUS UNIVERSITY   (Denmark)

^b BGI/HuaDa JiYin Shenzhen   (China)

Author keywords

Gene targeting; Genetically modified pigs; Homologous recombination; RAAV; SCNT

Indexed keywords

BRCA1 PROTEIN; PARVOVIRUS VECTOR;

DNA MODIFICATION; DOUBLE STRANDED DNA BREAK; FIBROBLAST; GENE TARGETING; GENETIC ENGINEERING AND GENE TECHNOLOGY; GENOME EDITING; NONHUMAN; PHENOTYPE; REVIEW; SWINE; VIRUS RECOMBINANT;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DEPENDOVIRUS; GENE TARGETING; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; NUCLEAR TRANSFER TECHNIQUES; SWINE;

ADENO-ASSOCIATED VIRUS; MAMMALIA; SUIDAE; SUS;

EID: 84863091853     PISSN: 16738527     EISSN: 18735533     Source Type: Journal    
DOI: 10.1016/j.jgg.2012.05.004     Document Type: Review

References (53)

1. Aigner B., Renner S., Kessler B., Klymiuk N., Kurome M., Wunsch A., Wolf E. Transgenic pigs as models for translational biomedical research. J. Mol. Med. 2010, 88:653-664.
2. Bode G., Clausing P., Gervais F., Loegsted J., Luft J., Nogues V., Sims J. The utility of the minipig as an animal model in regulatory toxicology. J. Pharmacol. Toxicol. Methods 2010, 62:196-220.
3. Bohenzky R.A., LeFebvre R.B., Berns K.I. Sequence and symmetry requirements within the internal palindromic sequences of the adeno-associated virus terminal repeat. Virology 1988, 166:316-327.
4. Brevini T.A., Antonini S., Pennarossa G., Gandolfi F. Recent progress in embryonic stem cell research and its application in domestic species. Reprod. Domest. Anim. 2008, 43(Suppl. 2):193-199.
5. Chen F., Pruett-Miller S.M., Huang Y., Gjoka M., Duda K., Taunton J., Collingwood T.N., Frodin M., Davis G.D. High-frequency genome editing using ssDNA oligonucleotides with zinc-finger nucleases. Nat. Methods 2011, 8:753-755.
6. Christian M., Cermak T., Doyle E.L., Schmidt C., Zhang F., Hummel A., Bogdanove A.J., Voytas D.F. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 2010, 186:757-761.
7. Du Y., Kragh P.M., Zhang Y., Li J., Schmidt M., Bogh I.B., Zhang X., Purup S., Jorgensen A.L., Pedersen A.M., Villemoes K., Yang H., Bolund L., Vajta G. Piglets born from handmade cloning, an innovative cloning method without micromanipulation. Theriogenology 2007, 68:1104-1110.
8. Ellis B.L., Hirsch M.L., Porter S.N., Samulski R.J., Porteus M.H. Zinc-finger nuclease-mediated gene correction using single AAV vector transduction and enhancement by food and drug administration-approved drugs. Gene Ther 2012, 10.1038/gt.2011.211.
9. Fattah F.J., Lichter N.F., Fattah K.R., Oh S., Hendrickson E.A. Ku70, an essential gene, modulates the frequency of rAAV-mediated gene targeting in human somatic cells. Proc. Natl. Acad. Sci. USA 2008, 105:8703-8708.
10. Grompe M., Al-Dhalimy M., Finegold M., Ou C.N., Burlingame T., Kennaway N.G., Soriano P. Loss of fumarylacetoacetate hydrolase is responsible for the neonatal hepatic dysfunction phenotype of lethal albino mice. Genes Dev. 1993, 7:2298-2307.
11. Guilbault C., Saeed Z., Downey G.P., Radzioch D. Cystic fibrosis mouse models. Am. J. Respir. Cell Mol. Biol. 2007, 36:1-7.
12. Hauschild J., Petersen B., Santiago Y., Queisser A.L., Carnwath J.W., Lucas-Hahn A., Zhang L., Meng X., Gregory P.D., Schwinzer R., Cost G.J., Niemann H. Efficient generation of a biallelic knockout in pigs using zinc-finger nucleases. Proc. Natl. Acad. Sci. USA 2011, 108:12013-12017.
13. Hickey R.D., Lillegard J.B., Fisher J.E., McKenzie T.J., Hofherr S.E., Finegold M.J., Nyberg S.L., Grompe M. Efficient production of Fah-null heterozygote pigs by chimeric adeno-associated virus-mediated gene knockout and somatic cell nuclear transfer. Hepatology 2011, 54:1351-1359.
14. Hirata R., Chamberlain J., Dong R., Russell D.W. Targeted transgene insertion into human chromosomes by adeno-associated virus vectors. Nat. Biotechnol. 2002, 20:735-738.
15. Hirata R.K., Russell D.W. Design and packaging of adeno-associated virus gene targeting vectors. J. Virol. 2000, 74:4612-4620.
16. Inoue N., Hirata R.K., Russell D.W. High-fidelity correction of mutations at multiple chromosomal positions by adeno-associated virus vectors. J. Virol. 1999, 73:7376-7380.
17. Keefer C.L., Pant D., Blomberg L., Talbot N.C. Challenges and prospects for the establishment of embryonic stem cell lines of domesticated ungulates. Anim. Reprod. Sci. 2007, 98:147-168.
18. Klymiuk N., Mundhenk L., Kraehe K., Wuensch A., Plog S., Emrich D., Langenmayer M.C., Stehr M., Holzinger A., Kroner C., Richter A., Kessler B., Kurome M., Eddicks M., Nagashima H., Heinritzi K., Gruber A.D., Wolf E. Sequential targeting of CFTR by BAC vectors generates a novel pig model of cystic fibrosis. J. Mol. Med. (Berl) 2011, 90:597-608.
19. Kohli M., Rago C., Lengauer C., Kinzler K.W., Vogelstein B. Facile methods for generating human somatic cell gene knockouts using recombinant adeno-associated viruses. Nucleic Acids Res. 2004, 32:e3.
20. Kragh P.M., Nielsen A.L., Li J., Du Y., Lin L., Schmidt M., Bogh I.B., Holm I.E., Jakobsen J.E., Johansen M.G., Purup S., Bolund L., Vajta G., Jorgensen A.L. Hemizygous minipigs produced by random gene insertion and handmade cloning express the Alzheimer's disease-causing dominant mutation APPsw. Transgenic Res. 2009, 18:545-558.
21. Kuzmuk K.N., Schook L.B. Pigs as a model for biomedical sciences. The Genetics of the Pigs 2011, 426. CAB International. M.F. Rothschild, A. Ruvinsky (Eds.).
22. Lai L., Prather R.S. Production of cloned pigs by using somatic cells as donors. Cloning Stem Cells 2003, 5:233-241.
23. Lai L., Kolber-Simonds D., Park K.W., Cheong H.T., Greenstein J.L., Im G.S., Samuel M., Bonk A., Rieke A., Day B.N., Murphy C.N., Carter D.B., Hawley R.J., Prather R.S. Production of alpha-1,3-galactosyltransferase knockout pigs by nuclear transfer cloning. Science 2002, 295:1089-1092.
24. Lindblad B., Lindstedt S., Steen G. On the enzymic defects in hereditary tyrosinemia. Proc. Natl. Acad. Sci. USA 1977, 74:4641-4645.
25. Linden R.M., Ward P., Giraud C., Winocour E., Berns K.I. Site-specific integration by adeno-associated virus. Proc. Natl. Acad. Sci. USA 1996, 93:11288-11294.
26. Liu X., Yan Z., Luo M., Zak R., Li Z., Driskell R.R., Huang Y., Tran N., Engelhardt J.F. Targeted correction of single-base-pair mutations with adeno-associated virus vectors under nonselective conditions. J. Virol. 2004, 78:4165-4175.
27. Luo Y., Bolund L., Sorensen C.B. Pig gene knockout by rAAV-mediated homologous recombination: comparison of BRCA1 gene knockout efficiency in Yucatan and Gottingen fibroblasts with slightly different target sequences. Transgenic Res. 2011, 21:671-676.
28. Luo Y., Li J., Liu Y., Lin L., Du Y., Li S., Yang H., Vajta G., Callesen H., Bolund L., Sorensen C.B. High efficiency of BRCA1 knockout using rAAV-mediated gene targeting: developing a pig model for breast cancer. Transgenic Res. 2011, 20:975-988.
29. Luo Y., Lin L., Bolund L., Jensen T.G., Sorensen C.B. Genetically modified pigs for biomedical research. J. Inherit. Metab. Dis 2012, 10.1007/s10545-012-9475-0.
30. Miller D.G., Petek L.M., Russell D.W. Human gene targeting by adeno-associated virus vectors is enhanced by DNA double-strand breaks. Mol. Cell Biol. 2003, 23:3550-3557.
31. Miller J.C., Tan S., Qiao G., Barlow K.A., Wang J., Xia D.F., Meng X., Paschon D.E., Leung E., Hinkley S.J., Dulay G.P., Hua K.L., Ankoudinova I., Cost G.J., Urnov F.D., Zhang H.S., Holmes M.C., Zhang L., Gregory P.D., Rebar E.J. A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 2011, 29:143-148.
32. Miyawaki K., Yamada Y., Yano H., Niwa H., Ban N., Ihara Y., Kubota A., Fujimoto S., Kajikawa M., Kuroe A., Tsuda K., Hashimoto H., Yamashita T., Jomori T., Tashiro F., Miyazaki J., Seino Y. Glucose intolerance caused by a defect in the entero-insular axis: a study in gastric inhibitory polypeptide receptor knockout mice. Proc. Natl. Acad. Sci. US A 1999, 96:14843-14847.
33. Muzyczka N. Use of adeno-associated virus as a general transduction vector for mammalian cells. Curr. Top. Microbiol. Immunol. 1992, 158:97-129.
34. Nakai H., Storm T.A., Kay M.A. Increasing the size of rAAV-mediated expression cassettes in vivo by intermolecular joining of two complementary vectors. Nat. Biotechnol. 2000, 18:527-532.
35. Paiboonsukwong K., Ohbayashi F., Shiiba H., Aizawa E., Yamashita T., Mitani K. Correction of mutant Fanconi anemia gene by homologous recombination in human hematopoietic cells using adeno-associated virus vector. J. Gene Med. 2009, 11:1012-1019.
36. Paulk N.K., Marquez Loza L., Finegold M., Grompe M. AAV-mediated gene targeting is significantly enhance by transient inhibition of NHEJ or the proteasome in vivo. Hum. Gene Ther 2012, 10.1089/hum.2012.038.
37. Pieroni L., Fipaldini C., Monciotti A., Cimini D., Sgura A., Fattori E., Epifano O., Cortese R., Palombo F., La Monica N. Targeted integration of adeno-associated virus-derived plasmids in transfected human cells. Virology 1998, 249:249-259.
38. Porteus M.H., Cathomen T., Weitzman M.D., Baltimore D. Efficient gene targeting mediated by adeno-associated virus and DNA double-strand breaks. Mol. Cell Biol. 2003, 23:3558-3565.
39. Prather R.S., Hawley R.J., Carter D.B., Lai L., Greenstein J.L. Transgenic swine for biomedicine and agriculture. Theriogenology 2003, 59:115-123.
40. Renner S., Fehlings C., Herbach N., Hofmann A., von Waldthausen D.C., Kessler B., Ulrichs K., Chodnevskaja I., Moskalenko V., Amselgruber W., Goke B., Pfeifer A., Wanke R., Wolf E. Glucose intolerance and reduced proliferation of pancreatic beta-cells in transgenic pigs with impaired glucose-dependent insulinotropic polypeptide function. Diabetes 2010, 59:1228-1238.
41. Riordan J.R., Rommens J.M., Kerem B., Alon N., Rozmahel R., Grzelczak Z., Zielenski J., Lok S., Plavsic N., Chou J.-L., Drumm M.L., Iannuzzi M.C., Collins F.S., Tsui L.-C. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 1989, 245:1066-1073.
42. Rogers C.S., Hao Y., Rokhlina T., Samuel M., Stoltz D.A., Li Y., Petroff E., Vermeer D.W., Kabel A.C., Yan Z., Spate L., Wax D., Murphy C.N., Rieke A., Whitworth K., Linville M.L., Korte S.W., Engelhardt J.F., Welsh M.J., Prather R.S. Production of CFTR-null and CFTR-DeltaF508 heterozygous pigs by adeno-associated virus-mediated gene targeting and somatic cell nuclear transfer. J. Clin. Invest. 2008, 118:1571-1577.
43. Rogers C.S., Stoltz D.A., Meyerholz D.K., Ostedgaard L.S., Rokhlina T., Taft P.J., Rogan M.P., Pezzulo A.A., Karp P.H., Itani O.A., Kabel A.C., Wohlford-Lenane C.L., Davis G.J., Hanfland R.A., Smith T.L., Samuel M., Wax D., Murphy C.N., Rieke A., Whitworth K., Uc A., Starner T.D., Brogden K.A., Shilyansky J., McCray P.B., Zabner J., Prather R.S., Welsh M.J. Disruption of the CFTR gene produces a model of cystic fibrosis in newborn pigs. Science 2008, 321:1837-1841.
44. Russell D.W., Hirata R.K. Human gene targeting by viral vectors. Nat. Genet. 1998, 18:325-330.
45. Tichy E.D., Pillai R., Deng L., Liang L., Tischfield J., Schwemberger S.J., Babcock G.F., Stambrook P.J. Mouse embryonic stem cells, but not somatic cells, predominantly use homologous recombination to repair double-strand DNA breaks. Stem Cells Dev. 2010, 19:1699-1711.
46. Trobridge G., Hirata R.K., Russell D.W. Gene targeting by adeno-associated virus vectors is cell-cycle dependent. Hum. Gene Ther 2005, 16:522-526.
47. Vajta G. Handmade cloning: the future way of nuclear transfer?. Trends Biotechnol 2007, 25:250-253.
48. Vajta G., Callesen H. Establishment of an efficient somatic cell nuclear transfer system for production of transgenic pigs. Theriogenology 2012, 77:1263-1274.
49. Vasileva A., Linden R.M., Jessberger R. Homologous recombination is required for AAV-mediated gene targeting. Nucleic Acids Res. 2006, 34:3345-3360.
50. Wernersson R., Schierup M.H., Jorgensen F.G., Gorodkin J., Panitz F., Staerfeldt H.H., Christensen O.F., Mailund T., Hornshoj H., Klein A., Wang J., Liu B., Hu S., Dong W., Li W., Wong G.K., Yu J., Bendixen C., Fredholm M., Brunak S., Yang H., Bolund L. Pigs in sequence space: a 0.66X coverage pig genome survey based on shotgun sequencing. BMC Genomics 2005, 6:70.
51. Wood A.J., Lo T.W., Zeitler B., Pickle C.S., Ralston E.J., Lee A.H., Amora R., Miller J.C., Leung E., Meng X., Zhang L., Rebar E.J., Gregory P.D., Urnov F.D., Meyer B.J. Targeted genome editing across species using ZFNs and TALENs. Science 2011, 333:307.
52. Wu Z., Yang H., Colosi P. Effect of genome size on AAV vector packaging. Mol. Ther. 2010, 18:80-86.
53. Yang J., Zhou W., Zhang Y., Zidon T., Ritchie T., Engelhardt J.F. Concatamerization of adeno-associated virus circular genomes occurs through intermolecular recombination. J. Virol. 1999, 73:9468-9477.