Genetic recombination pathways and their application for genome modification of human embryonic stem cells

Experimental Cell Research

Volumn 316, Issue 16, 2010, Pages 2578-2586

  Nieminen, Mikko ^a   Tuuri, Timo ^b,c   Savilahti, Harri ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

DNA transposition; Gene targeting; Homologous recombination; HR; Human embryonic stem cells; IPS cells; NHEJ; Non homologous end joining; Pluripotent; Site specific recombination

Indexed keywords

NUCLEASE; ZINC FINGER PROTEIN;

CELL LINE; DNA MODIFICATION; DNA TRANSPOSITION; EMBRYO; EMBRYONIC STEM CELL; GENE DELIVERY SYSTEM; GENE TARGETING; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW; TRANSPOSON; ADULT; CYTOLOGY; GENETIC ENGINEERING; GENETIC RECOMBINATION; HUMAN GENOME; METABOLISM; SIGNAL TRANSDUCTION;

EUKARYOTA;

ADULT; EMBRYONIC STEM CELLS; GENETIC ENGINEERING; GENOME, HUMAN; HUMANS; RECOMBINATION, GENETIC; SIGNAL TRANSDUCTION;

EID: 77955846843     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.06.004     Document Type: Review

References (59)

1. Pera M.F., Trounson A.O. Human embryonic stem cells: prospects for development. Development 2004, 131:5515-5525.
2. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
3. Zou J., Maeder M.L., Mali P., Pruett-Miller S.M., Thibodeau-Beganny S., Chou B.-K., Chen G., Ye Z., Park I.-H., Daley G.Q., Porteus M.H., Joung J.K., Cheng L. Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Cell Stem Cell 2009, 5:97-110.
4. Feng Q., Lu S.-J., Klimanskaya I., Gomes I., Kim D., Chung Y., Honig G.R., Kim K.-S., Lanza R. Hemangioblastic derivatives from human induced pluripotent stem cells exhibit limited expansion and early senescence. Stem cells 2010, 28:704-712.
5. Hu B.-Y., Weick J.P., Yu J., Ma L.-X., Zhang X.Q., Thomson J.A., Zhang S.-C. Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:4335-4340.
6. Leach D.R.F. Genetic recombination 1996, Blackwell Science, Oxford. 1st ed.
7. Brugmans L., Kanaar R., Essers J. Analysis of DNA double-strand break repair pathways in mice. Mutat. Res. 2007, 614:95-108.
8. Lieber M.R. The mechanism of human nonhomologous DNA end joining. J. Biol. Chem. 2008, 283:1-5.
9. Iiizumi S., Kurosawa A., So S., Ishii Y., Chikaraishi Y., Ishii A., Koyama H., Adachi N. Impact of non-homologous end-joining deficiency on random and targeted DNA integration: implications for gene targeting. Nucleic Acids Res. 2008, 36:6333-6342.
10. Pingoud A., Silva G.H. Precision genome surgery. Nat. Biotechnol. 2007, 25:743-744.
11. Song H., Chung S.-K., Xu Y. Modeling disease in human ESCs using an efficient BAC-based homologous recombination system. Cell Stem Cell 2010, 6:80-89.
12. Nolden L., Edenhofer F., Haupt S., Koch P., Wunderlich F.T., Siemen H., Brüstle O. Site-specific recombination in human embryonic stem cells induced by cell-permeant Cre recombinase. Nat. Meth. 2006, 3:461-467.
13. Paatero A.O., Turakainen H., Happonen L.J., Olsson C., Palomäki T., Pajunen M.I., Meng X., Otonkoski T., Tuuri T., Berry C., Malani N., Frilander M.J., Bushman F.D., Savilahti H. Bacteriophage Mu integration in yeast and mammalian genomes. Nucleic Acids Res. 2008, 36:e148.
14. Suzuki K., Mitsui K., Aizawa E., Hasegawa K., Kawase E., Yamagishi T., Shimizu Y., Suemori H., Nakatsuji N., Mitani K. Highly efficient transient gene expression and gene targeting in primate embryonic stem cells with helper-dependent adenoviral vectors. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:13781-13786.
15. Zeng J., Du J., Zhao Y., Palanisamy N., Wang S. Baculoviral vector-mediated transient and stable transgene expression in human embryonic stem cells. Stem Cells 2007, 25:1055-1061.
16. Lombardo A., Genovese P., Beausejour C.M., Colleoni S., Lee Y.-L., Kim K.A., Ando D., Urnov F.D., Galli C., Gregory P.D., Holmes M.C., Naldini L. Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat. Biotechnol. 2007, 25:1298-1306.
17. Gropp M., Itsykson P., Singer O., Ben-Hur T., Reinhartz E., Galun E., Reubinoff B.E. Stable genetic modification of human embryonic stem cells by lentiviral vectors. Mol. Ther. 2003, 7:281-287.
18. Gharwan H., Hirata R.K., Wang P., Richard R.E., Wang L., Olson E., Allen J., Ware C.B., Russell D.W. Transduction of human embryonic stem cells by foamy virus vectors. Mol. Ther. 2007, 15:1827-1833.
19. Mitsui K., Suzuki K., Aizawa E., Kawase E., Suemori H., Nakatsuji N., Mitani K. Gene targeting in human pluripotent stem cells with adeno-associated virus vectors. Biochem. Biophys. Res. Commun. 2009, 388:711-717.
20. Craig N.L. Unity in transposition reactions. Science 1995, 270:253-254.
21. Daya S., Cortez N., Berns K.I. Adeno-associated virus site-specific integration is mediated by proteins of the nonhomologous end-joining pathway. J. Virol. 2009, 83:11655-11664.
22. Giudice A., Trounson A. Genetic modification of human embryonic stem cells for derivation of target cells. Cell Stem Cell 2008, 2:422-433.
23. Braam S.R., Denning C., van den Brink S., Kats P., Hochstenbach R., Passier R., Mummery C.L. Improved genetic manipulation of human embryonic stem cells. Nat. Methods 2008, 5:389-392.
24. Hohenstein K.A., Pyle A.D., Chern J.Y., Lock L.F., Donovan P.J. Nucleofection mediates high-efficiency stable gene knockdown and transgene expression in human embryonic stem cells. Stem Cells 2008, 26:1436-1443.
25. Eiges R., Schuldiner M., Drukker M., Yanuka O., Itskovitz-Eldor J., Benvenisty N. Establishment of human embryonic stem cell-transfected clones carrying a marker for undifferentiated cells. Curr. Biol. 2001, 11:514-518.
26. Lakshmipathy U., Pelacho B., Sudo K., Linehan J.L., Coucouvanis E., Kaufman D.S., Verfaillie C.M. Efficient transfection of embryonic and adult stem cells. Stem Cells 2004, 22:531-543.
27. Siemen H., Nix M., Endl E., Koch P., Itskovitz-Eldor J., Brüstle O. Nucleofection of human embryonic stem cells. Stem Cells Dev. 2005, 14:378-383.
28. Cao F., Xie X.Y., Gollan T., Zhao L., Narsinh K., Lee R.J., Wu J.C. Comparison of gene-transfer efficiency in human embryonic stem cells. Mol. Imaging Biol. 2010, 12:15-24.
29. Cowan C.A., Klimanskaya I., McMahon J., Atienza J., Witmyer J., Zucker J.P., Wang S., Morton C.C., McMahon A.P., Powers D., Melton D.A. Derivation of embryonic stem-cell lines from human blastocysts. N. Engl. J. Med. 2004, 350:1353-1356.
30. Mikkola M., Olsson C., Palgi J., Ustinov J., Palomäki T., Horelli-Kuitunen N., Knuutila S., Lundin K., Otonkoski T., Tuuri T. Distinct differentiation characteristics of individual human embryonic stem cell lines. BMC Dev. Biol. 2006, 6:40.
31. Huangfu D., Osafune K., Maehr R., Guo W., Eijkelenboom A., Chen S., Muhlestein W., Melton D.A. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat. Biotechnol. 2008, 26:1269-1275.
32. Pyle A.D., Lock L.F., Donovan P.J. Neurotrophins mediate human embryonic stem cell survival. Nat. Biotechnol. 2006, 24:344-350.
33. Watanabe K., Ueno M., Kamiya D., Nishiyama A., Matsumura M., Wataya T., Takahashi J.B., Nishikawa S., Nishikawa S., Muguruma K., Sasai Y. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat. Biotechnol. 2007, 25:681-686.
34. Zwaka T.P., Thomson J.A. Homologous recombination in human embryonic stem cells. Nat. Biotechnol. 2003, 21:319-321.
35. Urbach A., Schuldiner M., Benvenisty N. Modeling for Lesch-Nyhan disease by gene targeting in human embryonic stem cell. Stem Cells 2004, 22:635-641.
36. Irion S., Luche H., Gadue P., Fehling H.J., Kennedy M., Keller G. Identification and targeting of the ROSA26 locus in human embryonic stem cells. Nat. Biotechnol. 2007, 25:1477-1482.
37. Costa M., Dottori M., Sourris K., Jamshidi P., Hatzistavrou T., Davis R., Azzola L., Jackson S., Lim S.M., Pera M., Elefanty A.G., Stanley E.G. A method for genetic modification of human embryonic stem cells using electroporation. Nat. Protoc. 2007, 2:792-796.
38. Davis R.P., Ng E.S., Costa M., Mossman A.K., Sourris K., Elefanty A.G., Stanley E.G. Targeting a GFP reporter gene to the MIXL1 locus of human embryonic stem cells identifies human primitive streak-like cells and enables isolation of primitive hematopoietic precursors. Blood 2008, 111:1876-1884.
39. Di Domenico A.I., Christodoulou I., Pells S.C., Mc Whir J., Thomson A.J. Sequential genetic modification of the hprt locus in human ESCs combining gene targeting and recombinase-mediated cassette exchange. Cloning and Stem Cells 2008, 10:217-229.
40. Xue H., Wu S., Papadeas S.T., Spusta S., Swistowska A.M., MacArthur C.C., Mattson M.P., Maragakis N.J., Capecchi M.R., Rao M.S., Zeng X., Liu Y. A targeted neuroglial reporter line generated by homologous recombination in human embryonic stem cells. Stem Cells 2009, 27:1836-1846.
41. Ruby K.M., Zheng B. Gene targeting in a HUES line of human embryonic stem cells via electroporation. Stem Cells 2009, 27:1496-1506.
42. Sakurai K., Shimoji M., Tahimic C.G.T., Aiba K., Kawase E., Hasegawa K., Amagai Y., Suemori H., Nakatsuji N. Efficient integration of transgenes into a defined locus in human embryonic stem cells. Nucleic Acids Res. 2010, 38:e96.
43. Copeland N.G., Jenkins N.A., Court D.L. Recombineering: a powerful new tool for mouse functional genomics. Nat. Rev. Genet. 2001, 2:769-779.
44. Hockemeyer D., Soldner F., Beard C., Gao Q., Mitalipova M., DeKelver R.C., Katibah G.E., Amora R., Boydston E.A., Zeitler B., Meng X., Miller J.C., Zhang L., Rebar E.J., Gregory P.D., Urnov F.D., Jaenisch R. Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat. Biotechnol. 2009, 27:851-857.
45. Thomson J.G., Ow D.W. Site-specific recombination systems for the genetic manipulation of eukaryotic genomes. Genesis 2006, 44:465-476.
46. Anastassiadis K., Fu J., Patsch C., Hu S., Weidlich S., Duerschke K., Buchholz F., Edenhofer F., Stewart A.F. Dre recombinase, like Cre, is a highly efficient site-specific recombinase in E. coli, mammalian cells and mice. Disease Models & Mechanisms 2009, 2:508-515.
47. Thyagarajan B., Liu Y., Shin S., Lakshmipathy U., Scheyhing K., Xue H., Ellerström C., Strehl R., Hyllner J., Rao M.S., Chesnut J.D. Creation of engineered human embryonic stem cell lines using phiC31 integrase. Stem Cells 2008, 26:119-126.
48. Ivics Z., Li M.A., Mátés L., Boeke J.D., Nagy A., Bradley A., Izsvák Z. Transposon-mediated genome manipulation in vertebrates. Nat. Methods. 2009, 6:415-422.
49. Wilber A., Linehan J.L., Tian X., Woll P.S., Morris J.K., Belur L.R., McIvor R.S., Kaufman D.S. Efficient and stable transgene expression in human embryonic stem cells using transposon-mediated gene transfer. Stem Cells 2007, 25:2919-2927.
50. Lacoste A., Berenshteyn F., Brivanlou A.H. An efficient and reversible transposable system for gene delivery and lineage-specific differentiation in human embryonic stem cells. Cell Stem Cell 2009, 5:332-342.
51. Mátés L., Chuah M.K., Belay E., Jerchow B., Manoj N., Acosta-Sanchez A., Grzela D.P., Schmitt A., Becker K., Matrai J., Ma L., Samara-Kuko E., Gysemans C., Pryputniewicz D., Miskey C., Fletcher B., Vandendriessche T., Ivics Z., Izsvák Z. Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nat. Genet. 2009, 41:753-761.
52. Vilen H., Eerikäinen S., Tornberg J., Airaksinen M., Savilahti H. Construction of gene-targeting vectors: a rapid Mu in vitro DNA transposition-based strategy generating null, potentially hypomorphic, and conditional alleles. Transgenic Res. 2001, 10:69-80.
53. Vallier L., Reynolds D., Pedersen R.A. Nodal inhibits differentiation of human embryonic stem cells along the neuroectodermal default pathway. Dev. Biol. 2004, 275:403-421.
54. Darr H., Mayshar Y., Benvenisty N. Overexpression of NANOG in human ES cells enables feeder-free growth while inducing primitive ectoderm features. Development 2006, 133:1193-1201.
55. Smith J.R., Maguire S., Davis L.A., Alexander M., Yang F., Chandran S., Ffrench-Constant C., Pedersen R.A. Robust, persistent transgene expression in human embryonic stem cells is achieved with AAVS1-targeted integration. Stem Cells 2008, 26:496-504.
56. Turakainen H., Saarimäki-Vire J., Sinjushina N., Partanen J., Savilahti H. Transposition-based method for the rapid generation of gene-targeting vectors to produce Cre/Flp-modifiable conditional knock-out mice. PLoS ONE 2009, 4:e4341.
57. Miller J.C., Holmes M.C., Wang J., Guschin D.Y., Lee Y.L., Rupniewski I., Beausejour C.M., Waite A.J., Wang N.S., Kim K.A., Gregory P.D., Pabo C.O., Rebar E.J. An improved zinc-finger nuclease architecture for highly specific genome editing. Nat. Biotechnol. 2007, 25:778-785.
58. Cornu T.I., Thibodeau-Beganny S., Guhl E., Alwin S., Eichtinger M., Joung J.K., Cathomen T. DNA-binding specificity is a major determinant of the activity and toxicity of zinc-finger nucleases. Mol. Ther. 2008, 16:352-358.
59. Petek L.M., Russell D.W., Miller D.G. Frequent endonuclease cleavage at off-target locations in vivo. Mol. Ther. 2010, 18:983-986.