Zinc-finger nuclease mediated disruption of Rag1 in the LEW/Ztm rat

BMC Immunology

Volumn 13, Issue , 2012, Pages

  Zschemisch, Nils Holger ^a   Glage, Silke ^a   Wedekind, Dirk ^a   Weinstein, Edward J ^b   Cui, Xiaoxia ^b   Dorsch, Martina ^a   Hedrich, Hans Jürgen ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b Sigma Aldrich Co   (United States)

Author keywords

Hypoplastic thymus; Lymphocytes; Natural killer cells; Rag1; Rat; Zinc finger nucleases

Indexed keywords

MESSENGER RNA; RAG1 PROTEIN; ZINC FINGER NUCLEASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BLOOD; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CODON; CONTROLLED STUDY; EMBRYO; FEMALE; FRAMESHIFT MUTATION; IMMUNOGLOBULIN PRODUCTION; INBRED STRAIN; LYMPH NODE; MALE; MICROINJECTION; NATURAL KILLER CELL; NONHUMAN; PROGENY; RAT; SPLEEN; T LYMPHOCYTE; THYMUS; ZYGOTE;

ALLELES; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; EMBRYO, MAMMALIAN; ENDONUCLEASES; FLOW CYTOMETRY; FRAMESHIFT MUTATION; GENE TARGETING; GENOTYPE; GERM CELLS; HOMEODOMAIN PROTEINS; HUMANS; LYMPHOCYTE DEPLETION; LYMPHOID TISSUE; MICE; MOLECULAR SEQUENCE DATA; RATS; RATS, INBRED LEW; RATS, MUTANT STRAINS; ZINC FINGERS;

EID: 84868499291     PISSN: None     EISSN: 14712172     Source Type: Journal    
DOI: 10.1186/1471-2172-13-60     Document Type: Article

References (52)

1. Charreau B, Tesson L, Soulillou JP, Pourcel C, Anegon I. Transgensis in rats: technical aspects and models. Transgenic Res 1996, 5:223-234. 10.1007/BF01972876, 8755162.
2. Jang CW, Behringer RR. Transposon-mediated transgensis in rats. CSH Protoc 2007,
3. Murphy D. Production of transgenic rodents by microinjection of cloned DNA into fertilized one-celled eggs. Methods Mol Biol 2008, 461:71-109. 10.1007/978-1-60327-483-8_7, 19030792.
4. Pfeifer A. Lentiviral transgenesis. Transgenic Res 2004, 13:513-522. 10.1007/s11248-004-2735-5, 15672832.
5. Tesson L, Cozzi J, Menoret S, Remy S, Usal C, Fraichard A, Anegon I. Transgenic modifications of the rat genome. Transgenic Res 2005, 14:531-546. 10.1007/s11248-005-5077-z, 16245144.
6. Ivics Z, Izsvak Z, Medrano G, Chapman KM, Hamra FK. Sleeping Beauty transposon mutagenesis in rat spermatogonial stem cells. Nat Prot 2011, 6:1521-1535.
7. Kitada K, Keng VW, Takeda J, Horie K. Generating mutant rats using the Sleeping Beauty transposon system. Methods 2009, 49:236-242. 10.1016/j.ymeth.2009.04.010, 19398007.
8. Li P, Tong C, Mehrian-Shai R, Jia L, Wu N, Yan Y, Maxson RE, Schulze EN, Song H, Hsieh C-L, Pera MF, Ying Q-L. Germline competent embryonic stem cells derived from rat blastocysts. Cell 2008, 135:1299-1310. 10.1016/j.cell.2008.12.006, 2735113, 19109898.
9. Buehr M, Meek S, Blair K, Yang J, Ure J, Silva J, McLay R, Hall J, Ying Q-L, Smith A. Capture of authentic embryonic stem cells from rat blastocysts. Cell 2008, 135:1287-1298. 10.1016/j.cell.2008.12.007, 19109897.
10. Meek S, Buehr M, Sunderlamd L, Thompson A, Mullins JJ, Smith AJ, Burdon T. Efficient gene targeting by homologous recombination in rat embryonic stem cells. PlosOne 2010, 5:e14225.
11. Tong C, Li P, Wu NL, Yan Y, Ying Q-L. Production of p53 gene knockout rats by homologous recombination in embryonic stem cells. Nature 2010, 467:211-213. 10.1038/nature09368, 2937076, 20703227.
12. Huang G, Chang T, Kumbhani DS, Ashton C, Yan H, Ying Q-L. Beyond knockout rats. New insights into finer genome manipulation in rats. Cell Cycle 2011, 10:1059-1066. 10.4161/cc.10.7.15233, 3100883, 21383544.
13. Yamamoto S, Nakata M, Sasada R, Ooshima Y, Yano T, Shinozawa T, Tsukimi Y, Takeyama M, Matsumoto Y, Hashimoto T. Derivation of rat embryonic stem cells and generation of protease-activated recepror-2 knockout rats. Transgenic Res 2011, epud anhead of print..
14. Urnov FD, Rebar FJ, Holmes MC, Zhang HS, Gregory PD. Genome editing with engenireed zinc finger nucleases. Nat Rev Genet 2010, 11:636-646. 10.1038/nrg2842, 20717154.
15. Li T, Huang S, Zhao X, Wright DA, Carpenter S, Spalding MH, Weeks DP, Yang B. Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res 2011, 39:6315-6325. 10.1093/nar/gkr188, 3152341, 21459844.
16. Remy S, Tesson L, Menoret S, Usal C, Scharenberg AM, Anegon I. Zinc-finger nucleases: a powerful tool for genetic engineering of animals. Transgenic Res 2010, 19:363-371. 10.1007/s11248-009-9323-7, 19821047.
17. Caroll D. Genome engineering with zinc-finger nucleases. Genetics 2011, 188:773-782. 10.1534/genetics.111.131433, 3176093, 21828278.
18. Connelly JP, Barker JC, Pruett-Miller S, Porteus MH. Gene correction by homologous recombination with zinc finger nucleases in primary cells from a mouse model of a generic recessive genetic disease. Mol Therapy 2010, 18:1103-1110.
19. Moehle EA, Rock JM, Lee Y-L, Jouvenot Y, DeKelver RC, Gregory PD, Urnov FD, Holmes MC. Targeted gene addition into a specified location in the human genome using designed zinc finger nucleases. Proc Natl Acad Sci USA 2007, 104:3055-3060. 10.1073/pnas.0611478104, 1802009, 17360608.
20. Santiago Y, Chan E, Liu P-Q, Orlando S, Zhang L, Urnov FD, Holmes MC, Guschin D, Waite A, Miller JC, Rebar EJ, Gregory PD, Klug A, Collingwood TN. Targeted gene knockout in mammalian cells using engineered zinc-finger nucleases. Proc Natl Acad Sci USA 2008, 105:5809-5814. 10.1073/pnas.0800940105, 2299223, 18359850.
21. Carbery ID, Ji D, Harrington A, Brown V, Weinstein EJ, Liaw L, Cui X. Targeted genome modification in mice using zinc-finger nucleases. Genetics 2010, 186:451-459. 10.1534/genetics.110.117002, 2954478, 20628038.
22. Ciu X, Ji D, Fisher DA, Wu Y, Briner DM, Weinstein EJ. Targeted integration in rat and mouse embryos with zinc-finger nucleases. Nat Biotech 2011, 29:64-67.
23. Meyer M, Hrabe De Angelis M, Wurst W, Kühn R. Gene targeting by homologous recombination in mouse zygotes mediated by zinc-finger nucleases. Proc Natl Acad Sci USA 2010, 107:15022-15026. 10.1073/pnas.1009424107, 2930558, 20686113.
24. Woods IG, Schier AF. Targeted mutagenesis in zebrafish. Nat Biotech 2008, 26:650-651.
25. Hauschild J, Petersen B, Santiago Y, Queisser A-L, Carnwath JW, Lucas-Hahn A, Zhang L, Meng X, Gregory PD, Schwinzer R, Cost GJ, Niemann H. Efficient generation of a biallelic knockout in pigs using zinc-finger nucleases. Proc Natl Acad Sci USA 2011, 108:12013-12017. 10.1073/pnas.1106422108, 3141985, 21730124.
26. Chu X, Zhang Z, Yabut J, Horwitz S, Levorse J, LI XQ, Zhu L, Ledermann H, Ortiga R, Strauss J, Li X, Owens KA, Dragovic J, Vogt T, Evers R, Shin MK. Characterization of multidrug resistance 1a/P-glycoprotein knockout rats generated by zinc finger nucleases. Mol Pharmacol 2012, 81:220-227. 10.1124/mol.111.074179, 22049154.
27. Guerts AM, Cost GJ, Freyvert Y, Zeitler B, Miller JC, Choi VM, Jenkins SS, Cui X, Meng X, Vincent A, Lam S, Michalkiewicz M, Schilling R, Foeckler J, Kalloway S, Weiler H, Menoret S, Anegon I, Davis GD, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Jacob HJ, Buelow R. Knockout rats via embryo microinjection of zinc-finger nucleases. Science 2009, 325:433. 10.1126/science.1172447, 2831805, 19628861.
28. Mashimo T, Takizawa A, Voigt B, Yoshimi K, Hiai H, Kuramoto T, Serikawa T. Generation of knockout rats with X-linked severe combined immunodeficiency (X-SCID) using zinc-finger nucleases. PlosONE 2010, 5:e8870.
29. Menoret S, Iscache A-L, Tesson L, Remy S, Usal C, Osborn MJ, Cost GJ, Brüggemann M, Buelow R, Anegon I. Characterization of immunoglobulin heavy chain knockout rats. Eur J Immunol 2010, 40:2932-2941. 10.1002/eji.201040939, 21038471.
30. Moreno C, Hoffman M, Stodola TJ, Didier DN, Lazar J, Guerts AM, North PE, Jacob HJ, Greene AS. Creation and characterization of a Renin knockout rat. Hypertension 2011, 57:614-9. 10.1161/HYPERTENSIONAHA.110.163840, 21242461.
31. Buckley RH. Molecular defects in human severe combined immunodeficiency and approaches to immune reconstitution. Ann Rev Immunol 2003, 22:625-655.
32. Niehues T, Perez-Becker R, Schuetz C. More than just SCID- the phenotypic range of combined immunodeficiencies associated with mutations in the recombinase activating genes (RAG) 1 and 2. Clin Immunol 2010, 135:183-192. 10.1016/j.clim.2010.01.013, 20172764.
33. Notarangelo LD, Villa A, Schwarz K. RAG and RAG defects. Curr Opin Immunol 1999, 11:435-442. 10.1016/S0952-7915(99)80073-9, 10448134.
34. Santagata S, Villa A, Sobacchi C, Cortes P, Vezzoni P. The genetic and biochemical basis of Omenn syndrome. Immunol Rev 2000, 178:64-74. 10.1034/j.1600-065X.2000.17818.x, 11213808.
35. Falk I, Potocnik AJ, Barthlott T, Levelt CN, Eichmann K. Immature T cells in peripheral lymphoid organs of the recombinase activating gene-1/-2- deficient mice. J Immunol 1996, 156:1362-1368.
36. Grundy MA, Sentman CL. Immunodeficient mice have elevated numbers of NK cells in non-lymphoid tissues. Exp Cell Res 2006, 312:3920-3926. 10.1016/j.yexcr.2006.08.019, 17005178.
37. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 1992, 68:869-877. 10.1016/0092-8674(92)90030-G, 1547488.
38. De P, Rodgers KK. Putting the pieces together: identification and characterization of structural domains in the V(D)J recombination protein RAG1. Immunlogical Reviews 2004, 200:70-82.
39. Oleykowski CA, Bronson Mullins CR, Godwin AK, Yeung AT. Mutation detection using a novel plant endonuclease. Nucleic Acids Res 1998, 26:4597-4602. 10.1093/nar/26.20.4597, 147896, 9753726.
40. Kulinski J, Besack D, Oleykowski CA, Godwin AK, Yeung AT. CEL I enzymatic mutation detection assay. Biotechniques 2000, 29(44-6):48.
41. Recillas-Targa F. Multiple strategies for gene transfer, expression, knockdown, and chromatin influence in mammalian cell lines and transgenic animals. Mol Biotechnol 2006, 34:337-354. 10.1385/MB:34:3:337, 17284781.
42. Filipiak WA, Saunders TL. Advances in transgenic rat production. Transgenic Res 2006, 15:673-686. 10.1007/s11248-006-9002-x, 17009096.
43. Sempirini S, Troup TJ, Kotelevtseva N, King K, Davis JR, Mullins LJ, Chapman KE, Dunbar DR, Mullins JJ. Cryptic loxP sites in mammalian genomes: genome-wide distribution and relevance for the efficiency of BAC/PAC recombineering techniques. Nucleic Acid Res 2007, 35:1402-1410. 10.1093/nar/gkl1108, 1865043, 17284462.
44. Schmidt EE, Taylor DS, Prigge JR, Barnett S, Carpecchi MR. Illegitimate Cre-dependent chromosome rearrangement in transgenic mouse spermatids. Proc Natl Acad Sci USA 2000, 97:13702-13707. 10.1073/pnas.240471297, 17639, 11087830.
45. Sigma Advanced Genetic Engineering Labs http://www.sageresearchmodels.com/research-models/knockout-rats/Rag1-knockout-rat)., Sigma Advanced Genetic Engineering Labs.
46. Bas A, Hammarström SG, Hammarström ML. Extrathymic TCG gene rearrangement in human small intestine: identification of new splice forms of recombinant activating gene-1 mRNA with selective tissue expression. J Immunol 2003, 171:3359-3371.
47. Collins C, Norris S, McEntee G, Traynor O, Bruno L, von Boehmer H, Hegarty J, Farrelly O. RAG1, RAG2 and pre-T cell receptor alpha chain expression by adult human hepatic T cells: evidence for extrathymic T cell maturation. Eur J Immunol 1996, 26:3114-3118. 10.1002/eji.1830261243, 8977312.
48. Ramanathan S, Marandi L, Poussier P. Evidence for the extrathymic origin of intestinal TCRγδ+ T cells in normal rats and for an impairment of this differentiation pathway in BB rats. J Immunol 2002, 168:2182-2187.
49. Santagata S, Gomez CA, Sobacchi C, Bozzi F, Abium M, Pasic S, Cortes P, Vezzoni P, Villa A. N-terminal RAG1 frameshift mutations in Omenn's syndrome: Internal methionine usage leads to partial V(D)J recombination activity and reveals a fundamental role in vivo for the N-terminal domains. Proc Natl Acad Sci USA 2000, 97:14572-14577. 10.1073/pnas.97.26.14572, 18960, 11121059.
50. Sobacchi C, Marella V, Rucci F, Vezzoni P, Villa A. RAG-dependent primary immunodeficiencies. Hum Mutat 2006, 12:1174-1184.
51. Nicklas W, Baneux P, Boot R, Decelle T, Deeny AA, Fumanelli M, Illgen-Wilcke B, FELASA (Federation of European Laboratory Animal Science Associations Working Group on Health Monitoring of Rodent and Rabbit Colonies) Recommendations for the health monitoring of rodent and rabbit colonies in breeding and experimental units. Lab Anim 2002, 6:20-42. FELASA (Federation of European Laboratory Animal Science Associations Working Group on Health Monitoring of Rodent and Rabbit Colonies).
52. Hamilton GC, Armstrong DT. The superovulation of synchronous adult rats using follicle-stimulation hormone delivered by continuous infusion. Biol Reprod 1991, 44:851-856. 10.1095/biolreprod44.5.851, 1907861.