Application of phiC31 integrase system in stem cells biology and technology: a review

References

• Belteki G, Gertsenstein M, Ow DW, Nagy A. 2003. Site-specific cassette exchange and germline transmission with mouse ES cells expressing ϕC31 integrase. Nature Biotech. 21(3):321–324. doi: 10.1038/nbt787
   Google Scholar
• Bi Y, Liu X, Zhang L, Shao C, Ma Z, Hua Z, Zhang L, Li L, Hua W, Xiao H, et al. 2013. Pseudo attP sites in favor of transgene integration and expression in cultured porcine cells identified by Streptomyces phage phiC31 integrase. BMC Mol Biol. 14(1):1–20. doi: 10.1186/1471-2199-14-20
   Google Scholar
• Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, Sedelnikova OA, Difilippantonio MJ, Redon C. 2002. Genomic instability in mice lacking histone H2AX. Science. 296(5569):922–927. doi: 10.1126/science.1069398
   Google Scholar
• Chalberg TW, Portlock JL, Olivares EC, Thyagarajan B, Kirby PJ, Hillman RT, Hoelters J, Calos MP. 2005. Φc31 integrase confers genomic integration and long-term transgene expression in rat retina. Invest Ophthalmol Vis Sci. 46(6):2140–2146. doi: 10.1167/iovs.04-1252
   Google Scholar
• Chalberg TW, Portlock JL, Olivares EC, Thyagarajan B, Kirby PJ, Hillman RT, Hoelters J, Calos MP. 2006. Integration specificity of phage φC31 integrase in the human genome. J Mol Biol. 357(1):28–48. doi: 10.1016/j.jmb.2005.11.098
   Google Scholar
• Chen C-m, Krohn J, Bhattacharya S, Davies B. 2011. A comparison of exogenous promoter activity at the ROSA26 locus using a phiC31 integrase mediated cassette exchange approach in mouse ES cells. PloS one. 6(8):1–8.
   Google Scholar
• Fontes A, Lakshmipathy U. 2013. Advances in genetic modification of pluripotent stem cells. Biotechnol Adv. 7:994–1001. doi: 10.1016/j.biotechadv.2013.07.003
   Google Scholar
• Fontes PA, Thomson AW. 1999. Stem cell technology. Br Med J. 319(7220):1308–1352. doi: 10.1136/bmj.319.7220.1308
   Google Scholar
• Gaj T, Gersbach CA, Barbas III CF. 2013. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends in Biotechnol. 7:397–405. doi: 10.1016/j.tibtech.2013.04.004
   Google Scholar
• Ghorbani R, Emamzadeh A, Khazaie Y, Dormiani K, Ghaedi K, Rabbani M, Foruzanfar M, Karbalaie K, Karamali F, Lachinani L, et al. 2013. Constructing a mouse Oct4 promoter/EGFP vector, as a whole-cellular reporter to monitor the pluripotent state of cells. Avicenna J Med Biotechnol. 5(1):2–9.
   Google Scholar
• Giudice A, Trounson A. 2008. Genetic modification of human embryonic stem cells for derivation of target cells. Cell Stem Cell. 2(5):422–433. doi: 10.1016/j.stem.2008.04.003
   Google Scholar
• Groth, AC, Olivares, EC, Thyagarajan, B, Calos, MP. (2000). A phage integrase directs efficient site-specific integration in human cells. Proc Natl Acad Sci USA,97(11), 5995–6000. doi: 10.1073/pnas.090527097
   Google Scholar
• Hockemeyer D, Wang H, Kiani S, Lai CS, Gao Q, Cassady JP, Cost GJ, Zhang L, Santiago Y, Miller JC, et al. 2011. Genetic engineering of human pluripotent cells using TALE nucleases. Nature Biotechnology. 29(8):731–734. doi: 10.1038/nbt.1927
   Google Scholar
• Hollis RP, Stoll SM, Sclimenti CR, Lin J, Chen-Tsai Y, Calos MP. 2003. Phage integrases for the construction and manipulation of transgenic mammals. Reprod Biol Endocrinol. 1(1):79–84. doi: 10.1186/1477-7827-1-79
   Google Scholar
• Holt N, Wang J, Kim K, Friedman G, Wang X, Taupin V, Crooks GM, Kohn DB, Gregory PD, Holmes MC, et al. 2010. Human hematopoietic stem/ progenitor cells modified by zinc-finger nucleases targeted to CCR5 control HIV-1 in vivo. Nature Biotechnol. 28(8):839–847. doi: 10.1038/nbt.1663
   Google Scholar
• Huang X, Guo H, Tammana S, Jung Y-C, Mellgren E, Bassi P, Cao Q, Tu ZJ, Kim YC, Ekker SC, et al. 2010. Gene transfer efficiency and genome-wide integration profiling of Sleeping Beauty, Tol2, and piggyBac transposons in human primary T cells. Mol Ther. 18(10):1803–1813. doi: 10.1038/mt.2010.141
   Google Scholar
• Imayoshi I, Hirano K, Kitano S, Miyachi H, Kageyama R. 2012. In vivo evaluation of phiC31 recombinase activity in transgenic mice. Neurosci Res. 73(2):106–114. doi: 10.1016/j.neures.2012.02.008
   Google Scholar
• Ishikawa Y, Tanaka N, Murakami K, Uchiyama T, Kumaki S, Tsuchiya S, Kugoh H, Oshimura M, Calos MP, Sugamura K. 2006. Phage ϕC31 integrase-mediated genomic integration of the common cytokine receptor gamma chain in human T-cell lines. J Gene Med. 8(5):646–653. doi: 10.1002/jgm.891
   Google Scholar
• Keravala A, Chavez C, Hu G, Woodard L, Monahan P, Calos M. 2011. Long-term phenotypic correction in factor IX knockout mice by using phiC31 integrase-mediated gene therapy. Gene Ther. 18(8):842–848. doi: 10.1038/gt.2011.31
   Google Scholar
• Keravala A, Hoelters J, Jarrahian S, Chalberg TW, Ciccarella M, Neth P, Calos MP. 2005. 1103. Site-specific chromosomal integration in human mesenchymal stem cells mediated by phiC31 integrase. Mol Ther. 11(S1):S425–S425.
   Google Scholar
• Keravala A, Ormerod BK, Palmer TD, Calos MP. 2008. Long-term transgene expression in mouse neural progenitor cells modified with φC31 integrase. J Neurosci Methods. 173(2):299–305. doi: 10.1016/j.jneumeth.2008.06.005
   Google Scholar
• Kong Q, Wu M, Huan Y, Zhang L, Liu H, Bou G, Liu Z, Mu Y, Liu Z. 2009. Transgene expression is associated with copy number and cytomegalovirus promoter methylation in transgenic pigs. PloS one. 4(8):1–10. doi: 10.1371/journal.pone.0006679
   Google Scholar
• Kuhstoss S, Rao RN. 1991. Analysis of the integration function of the streptomycete bacteriophage ϕC31. J Mol Biol. 222(4):897–908. doi: 10.1016/0022-2836(91)90584-S
   Google Scholar
• Lan F, Liu J, Narsinh KH, Hu S, Han L, Lee AS, Karow M, Nguyen PK, Nag D, Calos MP. 2012. Safe genetic modification of cardiac stem cells using a site-specific integration technique. Circulation. 126(11 Suppl. 1):S20–S28. doi: 10.1161/CIRCULATIONAHA.111.084913
   Google Scholar
• Leighton PA, van de Lavoir MC, Diamond JH, Xia C, Etches RJ. 2008. Genetic modification of primordial germ cells by gene trapping, gene targeting, and ϕC31 integrase. Mol Reprod Dev. 75(7):1163–1175. doi: 10.1002/mrd.20859
   Google Scholar
• Lieu PT, Machleidt T, Thyagarajan B, Fontes A, Frey E, Fuerstenau-Sharp M, Thompson DV, Swamilingiah GM, Derebail SS, Piper D, et al. 2009. Generation of site-specific retargeting platform cell lines for drug discovery using phiC31 and R4 integrases. J Biomol Screening. 14(10):1207–1215. doi: 10.1177/1087057109348941
   Google Scholar
• Liu J, Jeppesen I, Nielsen K, Jensen T. 2006. Φc31 integrase induces chromosomal aberrations in primary human fibroblasts. Gene Ther. 13(15):1188–1190. doi: 10.1038/sj.gt.3302789
   Google Scholar
• Liu J, Skjørringe T, Gjetting T, Jensen TG. 2009. PhiC31 integrase induces a DNA damage response and chromosomal rearrangements in human adult fibroblasts. BMC Biotechnol. 9(1):1–8. doi: 10.1186/1472-6750-9-31
   Google Scholar
• Ma Y, Ramezani A, Lewis R, Hawley RG, Thomson JA. 2003. High-level sustained transgene expression in human embryonic stem cells using lentiviral vectors. Stem Cells. 21(1):111–117. doi: 10.1634/stemcells.21-1-111
   Google Scholar
• Ma Q-w, Sheng H-q, Yan J-b, Cheng S, Huang Y, Chen-Tsai Y, Ren ZR, Huang SZ, Zeng YT. 2006. Identification of pseudo attP sites for phage φC31 integrase in bovine genome. Biochem Biophys Res Commun. 345(3):984–988. doi: 10.1016/j.bbrc.2006.04.145
   Google Scholar
• Merkl C, Saalfrank A, Riesen N, Kühn R, Pertek A, Eser S, Hardt MS, Kind A, Saur D, Wurst W. 2013. Efficient generation of rat induced pluripotent stem cells using a non-viral inducible vector. PloS one. 8(1):1–13. doi: 10.1371/journal.pone.0055170
   Google Scholar
• Nieminen M, Tuuri T, Savilahti H. 2010. Genetic recombination pathways and their application for genome modification of human embryonic stem cells. Exp Cell Res. 316(16):2578–2586. doi: 10.1016/j.yexcr.2010.06.004
   Google Scholar
• Nowakowski A, Andrzejewska A, Janowski M, Walczak P, Lukomska B. 2013. Genetic engineering of stem cells for enhanced therapy. Acta Neurobiol Exp. 73:1–18.
   Google Scholar
• Olivares EC, Hollis RP, Chalberg TW, Meuse L, Kay MA, Calos MP. 2002. Site-specific genomic integration produces therapeutic factor IX levels in mice. Nature Biotechnol. 20(11):1124–1128. doi: 10.1038/nbt753
   Google Scholar
• Orban TI, Apati A, Nemeth A, Varga N, Krizsik V, Schamberger A, Szebenyi K, Erdei Z, Várady G, Karaszi E, et al. 2009. Applying a “double-feature” promoter to identify cardiomyocytes differentiated from human embryonic stem cells following transposon-based gene delivery. Stem Cells. 27(5):1077–1087. doi: 10.1002/stem.45
   Google Scholar
• Ortiz-Urda S, Thyagarajan B, Keene DR, Lin Q, Calos MP, Khavari PA. 2003. Φc31 integrase-mediated nonviral genetic correction of junctional epidermolysis bullosa. Human Gene Therapy. 14(9):923–928. doi: 10.1089/104303403765701204
   Google Scholar
• Quenneville SP, Chapdelaine P, Rousseau J, Beaulieu J, Caron NJ, Skuk D, Mills P, Olivares ES, Calos PM, Tremblay JP. 2004. Nucleofection of muscle-derived stem cells and myoblasts with φC31 integrase: stable expression of a full-length-dystrophin fusion gene by human myoblasts. Mol Ther. 10(4):679–687. doi: 10.1016/j.ymthe.2004.05.034
   Google Scholar
• Quenneville SP, Chapdelaine P, Rousseau J, Tremblay JP. 2007. Dystrophin expression in host muscle following transplantation of muscle precursor cells modified with the phiC31 integrase. Gene Ther. 14(6):514–522. doi: 10.1038/sj.gt.3302887
   Google Scholar
• Rausch H, Lehmann M. 1991. Structural analysis of the actinophae ФC31 attachment site. Nucleic Acids Research. 19(19):5187–5189. doi: 10.1093/nar/19.19.5187
   Google Scholar
• Sivalingam J, Krishnan S, Ng WH, Lee SS, Phan TT, Kon OL. 2010. Biosafety assessment of site-directed transgene integration in human umbilical cord–lining cells. Mol Ther. 18(7):1346–1356. doi: 10.1038/mt.2010.61
   Google Scholar
• Smith M, Thorpe HM. 2002. Diversity in the serine recombinases. Mol Microbiol. 44(2):299–307. doi: 10.1046/j.1365-2958.2002.02891.x
   Google Scholar
• Tasic, B, Hippenmeyer, S, Wang, C, Gamboa, M, Zong, H, Chen-Tsai, Y, Luo, L. (2011). Site-specific integrase-mediated transgenesis in mice via pronuclear injection. Proc Natl Acad Sci USA, 108(19), 7902–7907. doi: 10.1073/pnas.1019507108
   Google Scholar
• Tenzen T, Zembowicz F, Cowan CA. 2010. Genome modification in human embryonic stem cells. J Cell Physiol. 222(2):278–281. doi: 10.1002/jcp.21948
   Google Scholar
• Thorpe HM, Smith MC. 1998. In vitro site-specific integration of bacteriophage DNA catalyzed by a recombinase of the resolvase/invertase family. Proc Natl Acad Sci USA. 95(10):5505–5510. doi: 10.1073/pnas.95.10.5505
   Google Scholar
• Thyagarajan B, Calos MP. 2005. Site-specific integration for high-level protein production in mammalian cells therapeutic proteins. California: Springer; p. 99–106.
   Google Scholar
• Thyagarajan B, Liu Y, Shin S, Lakshmipathy U, Scheyhing K, Xue H, Ellerström C, Strehl R, Hyllner J, Rao MS, et al. 2008. Creation of engineered human embryonic stem cell lines using phiC31 integrase. Stem Cells. 26(1):119–126. doi: 10.1634/stemcells.2007-0283
   Google Scholar
• Thyagarajan B, Olivares EC, Hollis RP, Ginsburg DS, Calos MP. 2001. Site-Specific Genomic Integration in Mammalian Cells Mediated by Phage φC31 Integrase. Mol Cell Biol. 21(12):3926–3934. doi: 10.1128/MCB.21.12.3926-3934.2001
   Google Scholar
• 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. 4:910–918. doi: 10.1016/j.cell.2013.04.025
   Google Scholar
• Wei Q-X, Odell AF, van der Hoeven F, Hollstein M. 2011. Rapid derivation of genetically related mutants from embryonic cells harboring a recombinase-specific Trp53 platform. Cell Cycle. 10(8):1261–1270. doi: 10.4161/cc.10.8.15303
   Google Scholar
• Wilber A, Linehan JL, Tian X, Woll PS, Morris JK, Belur LR, McIvor RS, Kaufman DS. 2007. Efficient and stable transgene expression in human embryonic stem cells using transposon-mediated gene transfer. Stem Cells. 25(11):2919–2927. doi: 10.1634/stemcells.2007-0026
   Google Scholar
• Wilber A, Ulloa Montoya F, Hammer L, Moriarity BS, Geurts AM, Largaespada DA, Verfaillie CM, McIvor RS, Lakshmipathy U. 2011. Efficient non-viral integration and stable gene expression in multipotent adult progenitor cells. Stem Cells International. 1:1–14. doi: 10.4061/2011/717069
   Google Scholar
• Ye, L, Chang, JC, Lin, C, Qi, Z, Yu, J, Kan, YW. (2010). Generation of induced pluripotent stem cells using site-specific integration with phage integrase. Proc Natl Acad Sci USA,107(45), 19467–19472. doi: 10.1073/pnas.1012677107
   Google Scholar
• Zhou Y-y, Zeng F. 2013. Integration-free methods for generating induced pluripotent stem cells. Genomics, Proteomics & Bioinformatics. 11(5):284–287. doi: 10.1016/j.gpb.2013.09.008
   Google Scholar
• Zhu F, Gamboa M, Farruggio AP, Hippenmeyer S, Tasic B, Schüle B, Chen-Tsai Y, Calos MP. 2014. DICE, an efficient system for iterative genomic editing in human pluripotent stem cells. Nucleic Acids Res. 42:1–13. doi: 10.1093/nar/gku978.
   Google Scholar