Enhancement of gene targeting in human cells by intranuclear permeation of the Saccharomyces cerevisiae Rad52 protein

Nucleic Acids Research

Volumn 38, Issue 14, 2010, Pages

  Kalvala, Arjun ^a,b,c   Rainaldi, Giuseppe ^b   di Primio, Cristina ^a   Liverani, Vania ^a   Falaschi, Arturo ^a,b,c   Galli, Alvaro ^b  

^a SCUOLA NORMALE SUPERIORE   (Italy)

^b CNR   (Italy)

^c INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; RAD52 PROTEIN; TRANSACTIVATOR PROTEIN; HYBRID PROTEIN; RAD52 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SINGLE STRANDED DNA;

ARTICLE; BINDING AFFINITY; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; DNA BINDING; DNA INTEGRATION; ESCHERICHIA COLI; GENE OVEREXPRESSION; HELA CELL; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; SACCHAROMYCES CEREVISIAE; SINGLE STRANDED DNA BREAK; ACTIVE TRANSPORT; BIOSYNTHESIS; CELL NUCLEUS; GENE TARGETING; GENETIC RECOMBINATION; GENETICS; HELA CELL LINE; METABOLISM; MUTATION; PROCEDURES;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL NUCLEUS; DNA, SINGLE-STRANDED; GENE TARGETING; HELA CELLS; HUMANS; MUTATION; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RECOMBINANT FUSION PROTEINS; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE PROTEINS; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

ESCHERICHIA COLI; SACCHAROMYCES CEREVISIAE;

EID: 77955838017     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq486     Document Type: Article

References (43)

1. Smith,K. (2001) Theoretical mechanisms in targeted and random integration of transgene DNA. Reprod. Nutr. Dev., 41, 465-485.
2. Rijkers,T., Van Den Ouweland,J., Morolli,B., Rolink,A.G., Baarends,W.M., Van Sloun,P.P., Lohman,P.H. and Pastink,A. (1998) Targeted inactivation of mouse RAD52 reduces homologous recombination but not resistance to ionizing radiation. Mol. Cell Biol., 18, 6423-6429.
3. Jasin,M. and Berg,P. (1988) Homologous integration in mammalian cells without target gene selection. Genes Dev., 2, 1353-1363.
4. Thomas,K.R., Deng,C. and Capecchi,M.R. (1992) High-fidelity gene targeting in embryonic stem cells by using sequence replacement vectors. Mol. Cell Biol., 12, 2919-2923.
5. Vispe,S., Cazaux,C., Lesca,C. and Defais,M. (1998) Overexpression of Rad51 protein stimulates homologous recombination and increases resistance of mammalian cells to ionizing radiation. Nucleic Acids Res., 26, 2859-2864.
6. Xia,S.J., Shammas,M.A. and Shmookler Reis,R.J. (1997) Elevated recombination in immortal human cells is mediated by HsRAD51 recombinase. Mol. Cell Biol., 17, 7151-7158.
7. Buerstedde,J.M. and Takeda,S. (1991) Increased ratio of targeted to random integration after transfection of chicken B cell lines. Cell, 67, 179-188.
8. Fattah,F.J., Lichter,N.F., Fattah,K.R., Oh,S. and Hendrickson,E.A. (2008) Ku70, an essential gene, modulates the frequency of rAAV-mediated gene targeting in human somatic cells. Proc. Natl Acad. Sci. USA, 105, 8703-8708.
9. Secretan,M.B., Scuric,Z., Oshima,J., Bishop,A.J., Howlett,N.G., Yau,D. and Schiestl,R.H. (2004) Effect of Ku86 and DNA-PKcs deficiency on non-homologous end-joining and homologous recombination using a transient transfection assay. Mutat. Res., 554, 351-364.
10. Aguilera,A. (1995) Genetic evidence for different RAD52-dependent intrachromosomal recombination pathways in Saccharomyces cerevisiae. Curr. Genet., 27, 298-305.
11. Galli,A., Cervelli,T. and Schiestl,R.H. (2003) Characterization of the hyperrecombination phenotype of the pol3-t mutation of Saccharomyces cerevisiae. Genetics, 164, 65-79.
12. Milne,G.T. and Weaver,D.T. (1993) Dominant negative alleles of RAD52 reveal a DNA repair/recombination complex including Rad51 and Rad52. Genes Dev., 7, 1755-1765.
13. Bai,Y., Davis,A.P. and Symington,L.S. (1999) A novel allele of RAD52 that causes severe DNA repair and recombination deficiencies only in the absence of RAD51 or RAD59. Genetics, 153, 1117-1130.
14. Yanez,R.J. and Porter,A.C. (2002) Differential effects of Rad52p overexpression on gene targeting and extrachromosomal homologous recombination in a human cell line. Nucleic Acids Res., 30, 740-748.
15. Park,M.S. (1995) Expression of human RAD52 confers resistance to ionizing radiation in mammalian cells. J. Biol. Chem., 270, 15467-15470.
16. Sugiyama,T., New,J.H. and Kowalczykowski,S.C. (1998) DNA annealing by RAD52 protein is stimulated by specific interaction with the complex of replication protein A and single-stranded DNA. Proc. Natl Acad. Sci. USA, 95, 6049-6054.
17. Shinohara,A., Shinohara,M., Ohta,T., Matsuda,S. and Ogawa,T. (1998) Rad52 forms ring structures and co-operates with RPA in single-strand DNA annealing. Genes Cells, 3, 145-156.
18. Mortensen,U.H., Erdeniz,N., Feng,Q. and Rothstein,R. (2002) A molecular genetic dissection of the evolutionarily conserved N terminus of yeast Rad52. Genetics, 161, 549-562.
19. Shi,I., Hallwyl,S.C., Seong,C., Mortensen,U., Rothstein,R. and Sung,P. (2009) Role of the Rad52 amino-terminal DNA binding activity in DNA strand capture in homologous recombination. J. Biol. Chem., 284, 33275-33284.
20. de Mayolo,A.A., Sunjevaric,I., Reid,R., Mortensen,U.H., Rothstein,R. and Lisby,M. (2010) The rad52-Y66A allele alters the choice of donor template during spontaneous chromosomal recombination. DNA Repair, 9, 23-32.
21. Van Dyck,E., Stasiak,A.Z., Stasiak,A. and West,S.C. (2001) Visualization of recombination intermediates produced by RAD52-mediated single-strand annealing. EMBO Rep., 2, 905-909.
22. Pohl,T.J. and Nickoloff,J.A. (2008) Rad51-independent interchromosomal double-strand break repair by gene conversion requires Rad52 but not Rad55, Rad57, or Dmc1. Mol. Cell Biol., 28, 897-906.
23. Haber,J.E. and Hearn,M. (1985) Rad52-independent mitotic gene conversion in Saccharomyces cerevisiae frequently results in chromosomal loss. Genetics, 111, 7-22.
24. Di Primio,C., Galli,A., Cervelli,T., Zoppe,M. and Rainaldi,G. (2005) Potentiation of gene targeting in human cells by expression of Saccharomyces cerevisiae Rad52. Nucleic Acids Res., 33, 4639-4648.
25. Frankel,A.D. and Pabo,C.O. (1988) Cellular uptake of the tat protein from human immunodeficiency virus. Cell, 55, 1189-1193.
26. Schwarze,S.R., Ho,A., Vocero-Akbani,A. and Dowdy,S.F. (1999) In vivo protein transduction: delivery of a biologically active protein into the mouse. Science, 285, 1569-1572.
27. Sonnemann,K.J., Heun-Johnson,H., Turner,A.J., Baltgalvis,K.A., Lowe,D.A. and Ervasti,J.M. (2009) Functional substitution by TAT-utrophin in dystrophin-deficient mice. PLoS Med., 6, e1000083.
28. Eguchi,A., Akuta,T., Okuyama,H., Senda,T., Yokoi,H., Inokuchi,H., Fujita,S., Hayakawa,T., Takeda,K., Hasegawa,M. et al. (2001) Protein transduction domain of HIV-1 Tat protein promotes efficient delivery of DNA into mammalian cells. J. Biol. Chem., 276, 26204-26210.
29. Yoneda,Y., Steiniger,S.C., Capkova,K., Mee,J.M., Liu,Y., Kaufmann,G.F. and Janda,K.D. (2008) A cell-penetrating peptidic GRP78 ligand for tumor cell-specific prodrug therapy. Bioorg. Med. Chem. Lett., 18, 1632-1636.
30. Morris,M.C., Deshayes,S., Heitz,F. and Divita,G. (2008) Cell-penetrating peptides: from molecular mechanisms to therapeutics. Biol. Cell, 100, 201-217.
31. Fittipaldi,A., Ferrari,A., Zoppe,M., Arcangeli,C., Pellegrini,V., Beltram,F. and Giacca,M. (2003) Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion proteins. J. Biol. Chem., 278, 34141-34149.
32. Cardarelli,F., Serresi,M., Bizzarri,R., Giacca,M. and Beltram,F. (2007) In vivo study of HIV-1 Tat arginine-rich motif unveils its transport properties. Mol. Ther., 15, 1313-1322.
33. Gustafsson,A.B., Sayen,M.R., Williams,S.D., Crow,M.T. and Gottlieb,R.A. (2002) TAT protein transduction into isolated perfused hearts: TAT-apoptosis repressor with caspase recruitment domain is cardioprotective. Circulation, 106, 735-739.
34. Vives,E., Brodin,P. and Lebleu,B. (1997) A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem., 272, 16010-16017.
35. Brooks,H., Lebleu,B. and Vives,E. (2005) Tat peptide-mediated cellular delivery: back to basics. Adv. Drug Deliv. Rev., 57, 559-577.
36. Cao,G., Pei,W., Ge,H., Liang,Q., Luo,Y., Sharp,F.R., Lu,A., Ran,R., Graham,S.H. and Chen,J. (2002) In vivo delivery of a Bcl-xL fusion protein containing the TAT protein transduction domain protects against ischemic brain injury and neuronal apoptosis. J. Neurosci., 22, 5423-5431.
37. Tasciotti,E., Zoppe,M. and Giacca,M. (2003) Transcellular transfer of active HSV-1 thymidine kinase mediated by an 11-amino-acid peptide from HIV-1 Tat. Cancer Gene Ther., 10, 64-74.
38. Sandgren,S., Cheng,F. and Belting,M. (2002) Nuclear targeting of macromolecular polyanions by an HIV-Tat derived peptide Role for cell-surface proteoglycans. J. Biol. Chem., 277, 38877-38883.
39. Kabouridis,P.S., Hasan,M., Newson,J., Gilroy,D.W. and Lawrence,T. (2002) Inhibition of NF-kappa B activity by a membrane-transducing mutant of I kappa B alpha. J. Immunol., 169, 2587-2593.
40. Song,B. and Sung,P. (2000) Functional interactions among yeast Rad51 recombinase, Rad52 mediator, and replication protein A in DNA strand exchange. J. Biol. Chem., 275, 15895-15904.
41. Dignam,J.D., Lebovitz,R.M. and Roeder,R.G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res., 11, 1475-1489.
42. Haglund,R.E. and Rothblum,L.I. (1987) Isolation, fractionation and reconstitution of a nuclear extract capable of transcribing ribosomal DNA. Mol. Cell Biochem., 73, 11-20.
43. Ciotta,C., Ceccotti,S., Aquilina,G., Humbert,O., Palombo,F., Jiricny,J. and Bignami,M. (1998) Increased somatic recombination in methylation tolerant human cells with defective DNA mismatch repair. J. Mol. Biol., 276, 705-719.