Intramolecular integration assay validates integrase PHI C31 and R4 potential in a variety of insect cells

Southeast Asian Journal of Tropical Medicine and Public Health

Volumn 40, Issue 6, 2009, Pages 1235-1253

  Chompoosri, Jakkrawarn ^a,b,d   Fraser, Tresa ^a   Rongsriyam, Yupha ^b   Komalamisra, Narumon ^b   Siriyasatien, Padet ^c   Thavara, Usavadee ^d   Tawatsin, Apiwat ^d   Fraser Jr , Malcolm J ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b MAHIDOL UNIVERSITY   (Thailand)

^c CHULALONGKORN UNIVERSITY   (Thailand)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 76749127516     PISSN: 01251562     EISSN: 26975718     Source Type: Journal    
DOI: None     Document Type: Article

References (107)

1. Allen BG, Weeks DL. Transgenic Xenopus laevis embryos can be generated using phiC31 integrase. Nat Methods 2005; 2: 975-979
2. Allen BG, Weeks DL. Bacteriophage phiC31 integrase mediated transgenesis in Xenopus laevis for protein expression at endogenous levels. Methods Mol Biol 2009; 518:113-122
3. Atkinson PW, Warren WD, O'Brochta DA. The hobo transposable element of Drosophila can be cross-mobilized in houseflies and excises like the Ac element of maize. Proc Natl Acad Sei USA 1993; 90: 9693-9697 (Pubitemid 23315852)
4. Bateman JR, Lee AM, Wu CT. Site-specific transformation of Drosophila via φC31 integrasemediated cassette exchange. Genetics 2006; 173: 769-777
5. Bateman JR, Wu CT. A simple polymerase chain reaction-based method for the construction of recombinase-mediated cassette exchange donor vectors. Genetics 2008; 180:1763-1766
6. Beall EL, Rio DC. Drosophila P-element transposase is a novel site-specific endonuclease. Genes Dev 1997; 11: 2137-2151
7. Belteki G, Gertsenstein M, Ow DW, Nagy A. Sitespecific cassette exchange and germlines transmission with mouse Es cells expressing φC31 integrase. Nature Biotechnol 2003; 21: 321-324 (Pubitemid 36314819)
8. Bertoni C, Jarrahian S, Wheeler TM, et al. Enhancement of plasmid-mediated gene therapy for muscular dystrophy by directed plasmid integration. Proc Natl Acad Sci USA 2006; 103: 419-424 (Pubitemid 43122416)
9. Bischof J, Maeda RK, Hediger M, Karch F, Basler K. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci USA 2007; 104: 3312-3317 (Pubitemid 46364156)
10. Bond BJ, Davidson N. The Drosophila melanogaster actin 5C gene uses two transcription initiation sites and three polyadenylation sites to express multiple mRNA species. Mol Cel Biol 1986; 6: 2080-2088
11. BrondstedL,HammerK. UseoftheintegrationelementsencodedbythetemperateIactococcalbacteriophageTP901-1- obtainchromosomalsingle-copytranscriptionalfusionsinLactococcuslactis. ApplEnvironMicrobiol1999;65:752-758(Pubitemid29075127)
12. Burn TC, Vigoreaux JO, Tobin SL. Alternative actin 5C transcripts are localized in different patterns during Drosophila embryogenesis. Dev Biol 1989; 131: 345-355
13. Campbell AM. Chromosomal insertion sites for phages and plasmids. J Bacteriol 1992; 174: 7495-7499
14. Cary LC, Goebel M, Corsaro BG, Wang HG, Rosen E, Fraser MJ. Transposon mutagenesis of Baculoviruses: Analysis of Trichoplusia ni transposon IFP2 insertions within the FPLocus of nuclear polyhedrosis viruses. Virology 1989; 172:156-169 (Pubitemid 19221445)
15. Chalberg TW, Genise HL, Vollrath D, Calos MP. phiC31 integrase confers genomic integration and long-term transgene expression in rat retina. Invest Ophthalmol Vis Sci 2005; 46: 2140-2146
16. ChristiansenB,BrondstedL,VogensenFK,HammerK.Aresolvase- likeproteinisrequiredforthesite- specificintegrationofthetemperateIactococcalbacteriophageTP901-1. JBacteriol1996;178:5164-5173(Pubitemid26293075)
17. ChungYT,KellerEB. Positiveandnegativeregulatoryelementsmediatingtranscriptionfromthe Drosophilamelanogasteractin5Cdistalpromoter.MolCellBiol1990;10: 6172-6180(Pubitemid120004559)
18. Coates CJ, Jasinskiene N, Miyashiro L, James AA. Mariner transposition and transformation of the yellow fever mosquito, Aedes aegypti. Proc Natl Acad Sci USA 1998; 95: 3748-3751 (Pubitemid 28173200)
19. Cobreros L, Fernandez-Minan A, Luque CM, Gonzalez-Reyes A, Martin-Bermudo MD. A role for the chaperone Hsp70 in the regulation of border cell migration in the Drosophila ovary. Mech Dev 2008; 125:1048-1058
20. Dai H, Jiang R, Wang J, et al. Development of heat shock inducible and inheritable RNAi sys- tem in silkworm. Biomol Eng 2007; 24: 625-630 (Pubitemid 350137893)
21. DiNoceraPP,DawidIB. TransientexpressionofgenesintroducedintoculturedcellsofDrosophila. ProcNatlAcadSciUSA1983;80:7095-7098(Pubitemid14207360)
22. ElickTA,BauserCA,FraserMJ. ExcisionofthepiggyBactransposableelementinvitrois apreciseeventthatisenhancedbytheexpressionofitsencodedtransposase. Genetica1996;98:33-41.(Pubitemid126705766)
23. Farhood H, Serbina N, Huang L. The role of dioleoyl- phosphatidylethanolamine in cationic liposome mediated gene transfer. Biochim Biophys Acta 1995; 1235: 289-295
24. FeignerJH,KumarR,SridharCN,etal. Enhancedgenedeliveryandmechanismstudieswithanovelseries ofcationiclipidformulations.JBiolChem1994;269:2550-2561(Pubitemid24235749)
25. Finnegan DJ. Transposable elements. Curr Opin Genet Dev 1992; 2: 861-867
26. Franz G, Savakis C. Minos, a new transposable element from Drosophila hydei, is a member of the Tc1-like family of transposons. Nucleic Acids Res 1991; 19: 6646.
27. Fraser MJ. The TTAA-specific family of transposable elements. Identification, functional characterization, and utility for transformation of insects. In: Handler AM, James AA, eds. Insect transgenesis, 2000: 249-268
28. FraserMJ,CiszczonT,ElickT,BauserC.PreciseexcisionofTTAA- specificlepidopterantransposonspiggyBac(IFP2)andtagalong.(TFP3) fromthebaculovirusgenomeincelllinesfromtwospeciesofLepidoptera. InsectMolBiol1996;5:141-151(Pubitemid2622611)
29. Fyrberg EA, Bond BJ, Hershey ND, Mixter KS, Davidson N. The actin genes of Drosophila: protein coding regions are highly conserved but intron positions are not. Cell 1981; 24: 107-116
30. Fyrberg EA, Mahaffey JW, Bond BJ, Davidson N. Transcripts of the six Drosophila actin genes accumulate in a stage- and tissue-specific manner. Cell 1983; 33:115-123
31. Grossman GL, Rafferty CS, Clayton JR, Stevens TK, Mukabayire O, Benedict MQ. Germline transformation of the malaria vector, Anopheles gambiae, with the piggyBac transposable element. Insect Mol Biol 2001; 10: 597-604. (Pubitemid 34010043)
32. Groth AC, Fish M, Nusse R, Calos MP. Construction of transgenic Drosophila by using the site-specific integrase from Phage φC31 integrase. Genetics 2004; 166:1775-1782 (Pubitemid 38621059)
33. Groth AC, Olivares EC, Thyagarajan B, Calos MP. A phage integrase directs efficient site-specific integration in human cells. Proc Natl Acad Sci USA 2000; 97: 5995-6000. (Pubitemid 30367512)
34. Guss AM, Rother M, Zhang JK, Kulkami G, Metcalf WW. New methods for tightly regulated gene expression and highly efficient chromosomal integration of cloned genes for Methanosarcina species. Archaea 2008; 2: 193-203.
35. Han K, Levine MS, Manley JL. Synergistic activation and repression of transcription by Drosophila homeobox proteins. Cell 1989; 56: 573-583 (Pubitemid 19065529)
36. Handler AM, Harrell RA. Germline transformation of Drosophila melanogaster with the piggyBac transposon vector. Insect Mol Biol 1999; 8: 449-457
37. Handler AM, Harrell RA. Transformation of the Caribbean fruit fly with a piggyBac transposon vector marked with polyubiquitin-regulated GFP. Insect Biochem Mol Biol 2001; 31: 201-207
38. Handler AM, McCombs SD. The piggyBac transposon mediates germ-line transformation in the Oriental fruit fly and closely related elements exist in its genome. Insect Mol Biol 2000; 9: 605-612
39. Handler AM, McCombs SD, Fraser MJ, Saul SH. The Lepidopteran transposon vector piggyBac, mediates germ-line transformation in the Mediterranean fruit fly. Proc Natl Acad Sci USA 1998; 95:7520-7525
40. Hediger M, Niessen M, Wimmer EA, Dubendorfer A, Bopp D. Genetic transformation of the housefly Musca domestica with the lepidopteran derived transposon piggyBac. Insect Mol Biol 2001; 10:113-119 (Pubitemid 32320267)
41. Held PK, Olivares EC, Aguilar CP, Finegold M, Calos MP, Grompe M. In vivo correction of murine hereditary tyrosinemia type I by phiC31 integrase-mediated gene delivery. Mol Ther 2005; 11: 399-408. (Pubitemid 40277316)
42. Helgen JC, Fallon AM. Polybrene-mediated transfection of cultured lepidopteran cells: induction of a Drosophila heat shock promoter. In Vitro Cell Dev Biol 1990; 26: 731-736
43. Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol 1967; 26: 365-369
44. Hollis RP, Stoll SM, Sclimenti CR, Lin J, ChenTsai Y, Calos MP. Phage integrases for the construction and manipulation of transgenic mammals. Reprod Biol Endocrinol 2003; 1:1-11.
45. Hong Y, Hondalus MK. Site-specific integration of Streptomyces φC31integrase-based vectors in the chromosome of Rhodococcus equi. FEMS Microbiol Lett 2008; 287: 63-68
46. Hui SW, Stewart TP, Boni LT, Yeagle PL. Membrane fusion through point defects in bilayers. Science 1981; 212: 921-923
47. Huynh CQ, Zieler H. Construction of modular and versatile plasmid vectors for the highlevel expression of single or multiple genes in insects and insect cell lines. J Mol Biol 1999; 288:13-20. (Pubitemid 29203750)
48. Keravala A, Ormerod BK, Palmer TD, Calos MP. Long-term transgene expression in mouse neural progenitor cells modified with phiC31 integrase. J Neurosci Methods 2008; 173: 299-305.
49. Kokoza V, Ahmed A, Wimmer EA, Raikhel AS. Efficient transformation of the yellow fever mosquito Aedes aegypti using the piggyBac transposable element vector pBac[3XP3EGFP afm]. Insect Biochem Mol Biol 2001; 31: 1137-1143 (Pubitemid 33032523)
50. KuhstossS,RaoRN. AnalysisoftheintegrationfunctionofthestreptomycetebacteriophagephiC31. JMolBiol1991;222:897-908.(Pubitemid121003478)
51. Legendre JY, Szoka FC Jr. Cyclic amphipathic peptide-DNA complexes mediate high-efficiency transfection of adherent mammalian cells. Proc Natl Acad Sci USA 1993; 90:893-897 (Pubitemid 23053916)
52. Linquist S, Craig EA. The heat shock proteins. Annu Rev Genet 1988; 22: 631-677
53. Lis JT, Simon JA, Sutton CA. New heat shock puffs and β-galactosidase activity resulting from transformation of Drosophila with an hsp70-LacZ hybrid gene. Cell 1983; 35:403-410
54. Lobo N, Hua-Van A, Li X, Nolen BM, Fraser MJ. Germ line transformation of the yellow fever mosquito, Aedes aegypti, mediated by transpositional insertion of a piggyBac vector. Insect Mol Biol 2002;11:133-139 (Pubitemid 34432238)
55. Lobo N, Li X, Fraser MJ. Transposition of the piggyBac element in embryos of Drosophila melanogaster, Aedes aegypti and Trichoplusia ni. Mol Gen Genet 1999; 261: 803-810 (Pubitemid 29286760)
56. LoboN,LiX,Hua-VanA,FraserMJ. MobilityofthepiggyBactransposoninembryosofthevectorsofDenguefever (Aedesalbopictus)andLaCrosseencephalitis(Ae.triseriatus).MoIGenetGenomics2001; 265:66-71.(Pubitemid32260799)
57. Lycett GJ, Crampton JM. Stable transformation of mosquito cell lines using a hsp70: neo fusion gene. Gene 1993; 136:129-136
58. Ma QW, Sheng HQ, Yan JB, et al. Identification of pseudo attP sites for phage phiC31 integrase in bovine genome. Biochem Biophys Res Commun 2006; 345: 984-988
59. MatsuuraM,NoguchiT,YamaguchiD,etal.Thesregene(ORF469)encodesasite- specificrecombinaseresponsibleforintegrationoftheR4phagegenome. JBacteriol1996;178:3374-3376(Pubitemid26169384)
60. Medhora M, Maruyama K, Hartl DL. Molecular and functional analysis of the mariner mutator element Mosl in Drosophila. Genetics 1991;128:311-318
61. Miller LH, Sakai RK, Romans P, Gwadz RW, Kantoff P, Coon HG. Stable integration and expression of a bacterial gene in the mosquito Anopheles gambiae. Science 1987; 237: 779-781
62. Morris AC, Eggleston P, Crampton JM. Genetic transformation of the mosquito Aedes aegypti by micro-injection of DNA. Med Vet Entomol 1989; 3:1-7.
63. Morris TD, Miller LK. Promoter influence on baculovirus-mediated gene expression in permissive and nonpermissive insect cell lines. J Virol 1992; 66: 7397-7405
64. Nakayama G, Kawaguchi Y, Koga K, Kusakabe T. Site-specific gene integration in cultured silkworm cells mediated by phiC31 integrase. Mol Genet Genomics 2006; 275: 1-8. (Pubitemid 43049986)
65. Nimmo DD, Alphey L, Meredith M, Eggleston P. High efficiency site-specific genetic engineering of the mosquito genome. Insect Mol Biol 2006; 15:129-136
66. Nolan T, Bower TM, Brown AE, Crisanti A, Catteruccia F. piggyBac-mediated germline transformation of the malaria mosquito Anopheles stephensi using the red fluorescent protein dsRED as a selectable marker. J Biol Chem 2002; 277: 8759-8762 (Pubitemid 34952938)
67. O'Brochta DA, Handler AM. Mobility of P elements in drosophilids and nondrosophilids. Proc Natl Acad Sci USA 1988; 85: 6052-6056
68. O'GormanS,FoxDT,WahlGM.Recombinasemediatedgeneactivationandsite- specificintegrationinmammaliancells.Science1991;251:1351-1355(Pubitemid21916917)
69. Olivares EC, Hollis RP, Chalberg TW, Meuse L, Kay MA, Calos MP. Site-specific genomic integration produces therapeutic Factor IX levels in mice. Nat Biotechnol 2002; 20:1124-1128 (Pubitemid 35285441)
70. Olivares EC, Hollis RP, Calos MP. Phage R4 integrase mediates site-specific integration in human cells. Gene 2001; 278:167-176
71. Ortiz-Urda S, Thyagarajan B, Keene DR, et al. Stable nonviral genetic correction of inherited human skin disease. Nat Med 2002; 8: 1166-1170 (Pubitemid 35175973)
72. Ortiz-Urda S, Thyagarajan B, Keene DR, Lin Q, Calos MP, Khavari PA. PhiC31 integrasemediated nonviral genetic correction of junctional epidermolysis bullosa. Hum Gene Ther 2003; 14: 923-928 (Pubitemid 36693800)
73. Ou HL, Huang Y, Qu LJ, et al. A phiC31 integrase-. mediated integration hotspot in favor of transgene expression exists in the bovine genome. FEBS J 2009; 276:155-163
74. Peloquin JJ, Thibault ST, Staten R, Miller TA. Germline transformation of pink bollworm (Lepidoptera:gelechiidae) mediated by the piggyBac transposable element. Insect Mol Biol 2000; 3: 323-333 (Pubitemid 30427926)
75. Perera OP, Harrell IR, Handler AM. Germline transformation of the South American malaria vector, Anopheles albimanus, with a piggyBaciEGFP transposon vector is routine and highly efficient. Insect Mol Biol 2002; 11: 291-297
76. Pinkerton AC, Michel K, O'Brochta DA, Atkinson PW. Green fluorescent protein as a genetic marker in transgenic Aedes aegypti. Insect Mol Biol 2000; 9:1-10. (Pubitemid 30121207)
77. Plymale R, Grove MJ, Cox-Foster D, Ostiguy N, Hoover K. Plant-mediated alteration of the peritrophic matrix and baculovirus infection in lepidopteran larvae. J Insect Physiol 2008; 54: 737-749
78. Quenneville SP, Chapdelaine P, Rousseau J, et al. Nucleofection of muscle-derived stem cells and myoblasts with phiC31 integrase: stable expression of a full-length-dystrophin fusion gene by human myoblasts. Mol Ther 2004; 10: 679-687 (Pubitemid 39272857)
79. RauschH,LehmannM.StructuralanalysisoftheactinophagephiC31attachmentsite. NucleicAcidsRes1991;19:5187-5189(Pubitemid21912909)
80. Remy JS, Sirlin C, Vierling P, et al. Gene transfer with a series of lipophilic DNA-binding molecules. Biocojug Chem 1994; 5: 647-654
81. Ritossa F A new puf. ng pattern induced by temperature shock and DNP in Drosophila. Experentia 1962; 18: 571-573
82. Rubtsova M, Kempe K, Gils A, Ismagul A, Weyen, J, Gils M. Expression of active Streptomyces phage phiC31 integrase in transgenic wheat plants. Plant Cell Rep 2008; 27: 1821-1831
83. Sah NK, Taneja TK, Pathak N, Begum R, Athar M, Hasnaia SE. The baculovirus antiapoptotic p35 gene also functions via an oxidant-dependent pathway. Proc Natl Acad Sci USA 1999; 96: 4838-4843 (Pubitemid 29214498)
84. Sarkar A, Yardley K, Atkinson PW, James AA, O'Brochta DA. Transposition of the Hermes' dement in embryos of the vector mosquito, Aedes aegypti. Insect Biochem Mol Biol 1997; 27: 359-363 (Pubitemid 27274313)
85. Sauer B Site-specific recombination: developments and applications. Curr Opin Biotechnol 1994; 5: 521-527
86. SauerB,HendersonN. TargetedinsertionofexogenousDNAintotheeukaryoticgenomebytheCrerecombinase. NewBiol1990;2:441-449(Pubitemid20235657)
87. Sethuraman N, Fraser MJ, Eggleston P, O'Brochta DA. Post-integration stability of piggyBac in Aedes aegypti. Insect Biochem Mol Biol 2007; 37: 941-951
88. Shirai M, Nara H, Sato A, Aida T, Takahashi H. Site-specific integration of the actinophage R4 genome into the chromosome of Streptomyces parvulus upon lysogenization. J Bacteriol 1991; 173: 4237-4239
89. Shotkoski F, Zhang HG, Jackson MB, FrenchConstant RH.Stable expression of insect GABA receptors in insect cell lines. Promoters for efficient expression of Drosophila and mosquito Rd1 GABA receptors in stably transformed mosquito cell lines. FEBS Lett 1996;380:257-262 (Pubitemid 126352609)
90. Siddique HR, Gupta SC, Mitra K, et al. Adverse effect of tannery waste leachates in transgenic Drosophila melanogaster: role of ROS in modulation of Hsp70, oxidative stress and apoptosis. J Appl Toxicol 2008; 28: 734-748
91. Singh MP, Reddy MM, Mathur N, Saxena DK, Chowdhuri DK. Induction of hsp70, hsp60, hsp83 and hsp26 and oxidative stress markers in benzene, toluene and xylene exposed Drosophila melanogaster: Role of ROS generation. Toxicol Appl Pharmacol 2008. [Epub ahead of print].
92. Smith MC, Thorpe HM. Diversity in the serine recombinases. Mol Microbiol 2002; 44: 299-307.
93. Sorrell DA, Kolb AF. Targeted modification of mammalian genomes. Biotechnol Adv 2005; 23:431-469
94. Spradling AC. P element-mediated transformation. In: Roberts DB, ed. Drosophila: A Practical Approch. Oxford: IRL Press, 1986:175-197
95. Stark WM, Boocock MR, Sherratt DJ. Catalysis by site specific recombinases. Trends Genet 1992;8:432-439
96. Steiler H, Pirrotta V Regulated expression of genes injected into early Drosophila embryos. EMBO J 1984; 3:165-173
97. Suzuki MG, Funaguma S, Kanda T, Tamura T, Shimada T. Role of the male BmDSX protein in the sexual differentiation of Bombyx mori. Evol Dev 2005; 7: 58-68. (Pubitemid 40210833)
98. Tamura T, Thibert C, Royer C, Kanda T, et al. Germline transformation of the silkworm Bombyx mori L. using a piggyBac transposonderived vector. Nat Biotechnol 2000; 1: 81-84
99. Thomason LC, Calendar R, Ow DW. Gene insertion and replacement in Schizosaccharomyces pombe mediated by the Streptomyces bacteriophage φC31 site-specific recombination system. Mol Genet Genomics 2001; 265: 1031-1038 (Pubitemid 32702176)
100. Thorpe HM, Smith MC. In vitro site-specific integration of bacteriophage DNA catalyzed by a recombinase of the resolvase/invertase family. Proc Natl Acad Sci USA 1998; 95:5505-5510 (Pubitemid 28224124)
101. Thyagarajan B, Calos MP. Site-specific integration for high-level protein production in mammalian cells. Methods Mol Biol 2005; 308: 99-106.
102. Thyagarajan B, Liu Y, Shin S, et al. Creation of engineered human embryonic stem cell lines using phiC31 integrase. Stem Cells 2008; 26: 119-126
103. Thyagarajan B, Olivares EC, Hollis RP, Ginsburg DS, Calos MP. Site-specific genomic integration in mammalian cells mediated by phage φC31 integrase. Mol Cell Biol 2001; 21: 3926-3934 (Pubitemid 32476454)
104. Windbichler N, Papathanos PA, Catteruccia F, Ranson H, Burt A, Crisanti A. Homing endonuclease mediated gene targeting in Anopheles gambiae cells and embryos. Nucleic Acids Res 2007; 35: 5922-5933 (Pubitemid 47506306)
105. Zhang Y, Zhang X, Xia H, et al. Quantitative analysis of cytoplasmic actin gene promoter and nuclear polyhedrosis virus immediateearly promoter activities in various tissues of silkworm Bombyx mori using recombinant Autographa californica nuclear polyhedrosis virus as vector. Acta Biochim Biophys Sin (Shanghai) 2008; 40: 533-538 (Pubitemid 351847342)
106. ZhaoYG,EgglestonP. Comparativeanalysisofpromotersfortransientgeneexpressioninculturedmosquitocells. InsectMolBiol1999;8:31-38(Pubitemid29032133)
107. Zhou X, Huang L. DNA transfection mediated by cationic liposomes containing lipopolylysine: characterization and mechanism of action. Biochim Biophys Acta 1994; 1189:195-203. (Pubitemid 24042719)