Quantitation of HIV DNA integration: Effects of differential integration site distributions on Alu-PCR assays

Journal of Virological Methods

Volumn 189, Issue 1, 2013, Pages 53-57

  Brady, Troy ^a   Kelly, Brendan J ^a   Male, Frances ^a   Roth, Shoshannah ^a   Bailey, Aubrey ^a   Malani, Nirav ^a   Gijsbers, Rik ^b   O'Doherty, Una ^a   Bushman, Frederic D ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Alu; Integration; LEDGF p75; Quantitative PCR; Taqman

Indexed keywords

VIRUS DNA;

ALU SEQUENCE; ARTICLE; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROVIRUS; QUANTITATIVE ANALYSIS; VIRUS DNA CELL DNA INTERACTION;

ALU ELEMENTS; CELL LINE; DNA, VIRAL; HELA CELLS; HIV INFECTIONS; HIV-1; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; PROVIRUSES; RNA INTERFERENCE; RNA, SMALL INTERFERING; VIRUS INTEGRATION;

EID: 84873650932     PISSN: 01660934     EISSN: 18790984     Source Type: Journal    
DOI: 10.1016/j.jviromet.2013.01.004     Document Type: Article

References (32)

1. Agosto L.M., Yu J.J., Dai J., Kaletsky R., Monie D., O'Doherty U. HIV-1 integrates into resting CD4+ T cells even at low inoculums as demonstrated with an improved assay for HIV-1 integration. Virology 2007, 368:60-72.
2. Barr S.D., Ciuffi A., Leipzig J., Shinn P., Ecker J.R., Bushman F.D. HIV integration site selection: targeting in macrophages and the effects of different routes of viral entry. Mol. Ther. 2006, 14:218-225.
3. Berry C., Hannenhalli S., Leipzig J., Bushman F.D. Selection of target sites for mobile DNA integration in the human genome. PLoS Comput. Biol. 2006, 2:e157.
4. Butler S.L., Hansen M.S., Bushman F.D. A quantitative assay for HIV DNA integration in vivo. Nat. Med. 2001, 7:631-634.
5. Butler S.L., Johnson E.P., Bushman F.D. HIV cDNA metabolism studied by fluorescence-monitored PCR: notable stability of two-LTR circles. J. Virol. 2002, 76:3739-3747.
6. Cherepanov P., Devroe E., Silver P.A., Engelman A. Identification of an evolutionarily conserved domain in human lens epithelium-derived growth factor/transcriptional co-activator p75 (LEDGF/p75) that binds HIV-1 integrase. J. Biol. Chem. 2004, 279:48883-48892.
7. Cherepanov P., Maertens G., Proost P., Devreese B., Van Beeumen J., Engelborghs Y., De Clercq E., Debyser Z. HIV-1 integrase forms stable tetramers and associates with LEDGF/p75 protein in human cells. J. Biol. Chem. 2003, 278:372-381.
8. Ciuffi A., Diamond T.L., Hwang Y., Marshall H.M., Bushman F.D. Modulating target site selection during human immunodeficiency virus DNA integration in vitro with an engineered tethering factor. Hum. Gene Ther. 2006, 17:960-967.
9. Ciuffi A., Llano M., Poeschla E., Hoffmann C., Leipzig J., Shinn P., Ecker J.R., Bushman F. A role for LEDGF/p75 in targeting HIV DNA integration. Nat. Med. 2005, 11:1287-1289.
10. Ciuffi A., Ronen K., Brady T., Malani N., Wang G., Berry C.C., Bushman F.D. Methods for integration site distribution analyses in animal cell genomes. Methods 2009, 47:261-268.
11. Emiliani S., Mousnier A., Busschots K., Maroun M., Van Maele B., Tempe D., Vandekerckhove L., Moisant F., Ben-Slama L., Witvrouw M., Christ F., Rain J.C., Dargemont C., Debyser Z., Benarous R. Integrase mutants defective for interaction with LEDGF/p75 are impaired in chromosome tethering and HIV-1 replication. J. Biol. Chem. 2005, 280:25517-25523.
12. Farnet C.M., Haseltine W.A. Circularization of human immunodeficiency virus type 1 DNA in vitro. J. Virol. 1991, 65:6942-6952.
13. Ferris A.L., Wu X., Hughes C.M., Stewart C., Smith S.J., Milne T.A., Wang G.G., Shun M.-C., Allis C.D., Engelman A., Hughes S.H. Lens epithelium-derived growth factor fusion proteins redirect HIV-1 DNA integration. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:3135-3140.
14. Gijsbers R., Ronen K., Vets S., Malani N., De Rijck J., McNeely M., Bushman F.D., Debyser Z. LEDGF hybrids efficiently retarget lentiviral integration into heterochromatin. Mol. Ther. 2010, 18:552-560.
15. Humeau L.M., Binder G.K., Lu X., Slepushkin V., Merling R., Echeagaray P., Pereira M., Slepushkina T., Barnett S., Dropulic L.K., Carroll R., Levine B.L., June C.H., Dropulic B. Efficient lentiviral vector-mediated control of HIV-1 replication in CD4 lymphocytes from diverse HIV+ infected patients grouped according to CD4 count and viral load. Mol. Ther. 2004, 9:902-913.
16. Lander E. Initial sequencing and analysis of the human genome. Nature 2001, 409:860-921.
17. Llano M., Saenz D.T., Meehan A., Wongthida P., Peretz M., Walker W.H., Teo W., Poeschla E.M. An essential role for LEDGF/p75 in HIV integration. Science 2006, 314:461-464.
18. Lu X., Humeau L., Slepushkin V., Binder G., Yu Q., Slepushkina T., Chen Z., Merling R., Davis B., Chang Y.-N., Dropulic B. Safe two-plasmid production for the first clinical lentivirus vector that achieves >99% transduction in primary cells using a one-step protocol. J. Gene Med. 2004, 6:963-973.
19. Lu X., Yu Q., Binder G.K., Chen Z., Slepushkina T., Rossi J., Dropulic B. Antisense-mediated inhibition of human immunodeficiency virus (HIV) replication by use of an HIV type 1-based vector results in severely attenuated mutants incapable of developing resistance. J. Virol. 2004, 78:7079-7088.
20. Maertens G., Cherepanov P., Pluymers W., Busschots K., De Clercq E., Debyser Z., Engelborghs Y. LEDGF/p75 is essential for nuclear and chromosomal targeting of HIV-1 integrase in human cells. J. Biol. Chem. 2003, 278:33528-33539.
21. Marshall H.M., Ronen K., Berry C., Llano M., Sutherland H., Saenz D., Bickmore W., Poeschla E., Bushman F.D. Role of PSIP1/LEDGF/p75 in lentiviral infectivity and integration targeting. PLoS ONE 2007, 2:e1340.
22. Meylan S., Groner A.C., Ambrosini G., Malani N., Quenneville S., Zangger N., Kapopoulou A., Kauzlaric A., Rougemont J., Ciuffi A., Bushman F.D., Bucher P., Trono D. A gene-rich, transcriptionally active environment and the pre-deposition of repressive marks are predictive of susceptibility to KRAB/KAP1-mediated silencing. BMC Genomics 2011, 12:378.
23. O'Doherty U., Swiggard W.J., Jeyakumar D., McGain D., Malim M.H. A sensitive, quantitative assay for human immunodeficiency virus type 1 integration. J. Virol. 2002, 76:10942-10950.
24. Ocwieja K.E., Brady T.L., Ronen K., Huegel A., Roth S.L., Schaller T., James L.C., Towers G.J., Young J.A.T., Chanda S.K., König R., Malani N., Berry C.C., Bushman F.D. HIV integration targeting: a pathway involving transportin-3 and the nuclear pore protein RanBP2. PLoS Pathog. 2011, 7:e1001313.
25. Schaller T., Ocwieja K.E., Rasaiyaah J., Price A.J., Brady T.L., Roth S.L., Hue S., Fletcher A.J., Lee K., KewalRamani V.N., Noursadeghi M., Jenner R.G., James L.C., Bushman F.D., Towers G.J. HIV-1 capsid-cyclophilin interactions determine nuclear import pathway, integration targeting and replication efficiency. PLoS Pathog. 2011, 7:e1002439.
26. Schröder A.R.W., Shinn P., Chen H., Berry C., Ecker J.R., Bushman F. HIV-1 integration in the human genome favors active genes and local hotspots. Cell 2002, 110:521-529.
27. Shun M.-C., Raghavendra N.K., Vandegraaff N., Daigle J.E., Hughes S., Kellam P., Cherepanov P., Engelman A. LEDGF/p75 functions downstream from preintegration complex formation to effect gene-specific HIV-1 integration. Genes Dev. 2007, 21:1767-1778.
28. Silvers R.M., Smith J.A., Schowalter M., Litwin S., Liang Z., Geary K., Daniel R. Modification of integration site preferences of an HIV-1-based vector by expression of a novel synthetic protein. Hum. Gene Ther. 2010, 21:337-349.
29. Turlure F., Devroe E., Silver P.A., Engelman A. Human cell proteins and human immunodeficiency virus DNA integration. Front Biosci. 2004, 9:3187-3208.
30. Venter J.C. The sequence of the human genome. Science 2001, 291:1304-1351.
31. Wang G.P., Ciuffi A., Leipzig J., Berry C.C., Bushman F.D. HIV integration site selection: analysis by massively parallel pyrosequencing reveals association with epigenetic modifications. Genome Res. 2007, 17:1186-1194.
32. Wang Z., Zang C., Rosenfeld J.A., Schones D.E., Barski A., Cuddapah S., Cui K., Roh T.-Y., Peng W., Zhang M.Q., Zhao K. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 2008, 40:897-903.