Adeno-associated virus type 2 wild-type and Vector-Mediated genomic integration profiles of human diploid fibroblasts analyzed by third-generation PacBio DNA sequencing

Journal of Virology

Volumn 88, Issue 19, 2014, Pages 11253-11263

  Hu¨ser, Daniela ^a   Gogol Do¨ring, Andreas ^b,c,d   Chen, Wei ^b   Heilbronn, Regine ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c GERMAN CENTRE FOR INTEGRATIVE BIODIVERSITY RESEARCH IDIV HALLE JENA LEIPZIG   (Germany)

^d MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA;

ADENO ASSOCIATED VIRUS; ARTICLE; BRAIN; CHROMATIN; CONTROLLED STUDY; DIPLOIDY; DNA SEQUENCE; EMBRYONIC STEM CELL; FIBROBLAST; HEART; HELA CELL LINE; HUMAN; HUMAN CELL; LIVER; MUSCLE; NONHUMAN; NUCLEOTIDE SEQUENCE; SKIN; VIRUS DNA CELL DNA INTERACTION; VIRUS GENOME; ANTIBODY SPECIFICITY; CHEMISTRY; CYTOLOGY; FETUS; GENE VECTOR; GENETIC RECOMBINATION; GENETICS; HIGH THROUGHPUT SEQUENCING; LUNG; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE MOTIF; VIROLOGY;

CHROMATIN; DEPENDOVIRUS; DIPLOIDY; FETUS; FIBROBLASTS; GENETIC VECTORS; HELA CELLS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; LUNG; MOLECULAR SEQUENCE DATA; NUCLEOTIDE MOTIFS; ORGAN SPECIFICITY; RECOMBINATION, GENETIC; VIRUS INTEGRATION;

EID: 84906975820     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01356-14     Document Type: Article

References (41)

1. Muzyczka N, Berns KI. 2001. Parvoviridae: the viruses and their replication, p 2327-2359. In Knipe DM, Howley PM (ed), Fields virology, vol 2. Lippincott, Philadelphia, PA.
2. Kotin RM, Siniscalco M, Samulski RJ, Zhu XD, Hunter L, Laughlin CA, McLaughlin S, Muzyczka N, Rocchi M, Berns KI. 1990. Site-specific integration by adeno-associated virus. Proc. Natl. Acad. Sci. U. S. A. 87: 2211-2215. http://dx.doi.org/10.1073/pnas.87.6.2211.
3. Linden RM, Winocour E, Berns KI. 1996. The recombination signals for adeno-associated virus site-specific integration. Proc. Natl. Acad. Sci. U. S. A. 93:7966-7972. http://dx.doi.org/10.1073/pnas.93.15.7966.
4. Snyder RO, Im D-S, Ni T, Xiao X, Samulski RJ, Muzyczka N. 1993. Features of the adeno-associated virus origin involved in substrate recognition by the viral Rep protein. J. Virol. 67:6096-6104.
5. Im D-S, Muzyczka N. 1990. The AAV origin-binding protein Rep68 is an ATP-dependent site-specific endonuclease with helicase activity. Cell 61: 447-457. http://dx.doi.org/10.1016/0092-8674(90)90526-K.
6. Samulski RJ, Zhu X, Xiao X, Brook JD, Housman DE, Epstein N, Hunter LA. 1991. Targeted integration of adeno-associated virus (AAV) into human chromosome 19. EMBO J. 10:3941-3950. (Erratum, 11:1228, 1992.)
7. Kotin RM, Linden RM, Berns KI. 1992. Characterization of a preferred site on human chromosome 19q for integration of adeno-associated virus DNA by non-homologous recombination. EMBO J. 11:5071-5078.
8. Weitzman MD, Kyo¨stio¨ SRM, Kotin RM, Owens RA. 1994. Adenoassociated virus (AAV) Rep. proteins mediate complex formation between AAVDNAand its integration site in human DNA. Proc. Natl. Acad. Sci. U. S. A. 91:5808-5812. http://dx.doi.org/10.1073/pnas.91.13.5808.
9. Meneses P, Berns KI, Winocour E. 2000. DNA sequence motifs which direct adeno-associated virus site-specific integration in a model system. J. Virol. 74:6213-6216. http://dx.doi.org/10.1128/JVI.74.13.6213-6216.2000.
10. Hu¨ser D, Weger S, Heilbronn R. 2002. Kinetics and frequency of adenoassociated virus site-specific integration into human chromosome 19 monitored by quantitative real-time PCR. J. Virol. 76:7554-7559. http: //dx.doi.org/10.1128/JVI.76.15.7554-7559.2002.
11. Hu¨ser D, Heilbronn R. 2003. Adeno-associated virus integrates sitespecifically into human chromosome 19 in either orientation and with equal kinetics and frequency. J. Gen. Virol. 84:133-137. http://dx.doi.org /10.1099/vir.0.18726-0.
12. McCarty DM, Young SM, Jr., Samulski RJ. 2004. Integration of adenoassociated virus (AAV) and recombinant AAV vectors. Annu. Rev. Genet. 38:819-845. http://dx.doi.org/10.1146/annurev.genet.37.110801.143717.
13. Miller DG, Trobridge GD, Petek LM, Jacobs MA, Kaul R, Russell DW. 2005. Large-scale analysis of adeno-associated virus vector integration sites in normal human cells. J. Virol. 79:11434-11442. http://dx.doi.org /10.1128/JVI.79.17.11434-11442.2005.
14. Kaeppel C, Beattie SG, Fronza R, van Logtenstein R, Salmon F, Schmidt S, Wolf S, Nowrouzi A, Glimm H, von Kalle C, Petry H, Gaudet D, Schmidt M. 2013. A largely random AAV integration profile after LPLD gene therapy. Nat. Med. 19:889-891. http://dx.doi.org/10.1038/nm.3230.
15. Recchia A, Perani L, Sartori D, Olgiati C, Mavilio F. 2004. Site-specific integration of functional transgenes into the human genome by adeno/ AAV hybrid vectors. Mol. Ther. 10:660-670. http://dx.doi.org/10.1016/j .ymthe.2004.07.003.
16. Zhang C, Cortez NG, Berns KI. 2007. Characterization of a bipartite recombinant adeno-associated viral vector for site-specific integration. Hum. Gene Ther. 18:787-797. http://dx.doi.org/10.1089/hum.2007.056.
17. Wang H, Lieber A. 2006. A helper-dependent capsid-modified adenovirus vector expressing adeno-associated virus rep78 mediates site-specific integration of a 27-kilobase transgene cassette. J. Virol. 80:11699-11709. http://dx.doi.org/10.1128/JVI.00779-06.
18. Howden SE, Voullaire L, Wardan H, Williamson R, Vadolas J. 2008. Site-specific, Rep.-mediated integration of the intact beta-globin locus in the human erythroleukaemic cell line K562. Gene Ther. 15:1372-1383. http://dx.doi.org/10.1038/gt.2008.84.
19. Hu¨ser D, Gogol-Do¨ring A, Lutter T, Weger S, Winter K, Hammer EM, Cathomen T, Reinert K, Heilbronn R. 2010. Integration preferences of wild-type AAV-2 for consensus rep-binding sites at numerous loci in the human genome. PLoS Pathog. 6:e1000985. http://dx.doi.org/10.1371 /journal.ppat.1000985.
20. Janovitz T, Klein IA, Oliveira T, Mukherjee P, Nussenzweig MC, Sadelain M, Falck-Pedersen E. 2013. High-throughput sequencing reveals principles of adeno-associated virus serotype 2 integration. J. Virol. 87:8559-8568. http://dx.doi.org/10.1128/JVI.01135-13.
21. Macville M, Schrock E, Padilla-Nash H, Keck C, Ghadimi BM, Zimonjic D, Popescu N, Ried T. 1999. Comprehensive and definitive molecular cytogenetic characterization of HeLa cells by spectral karyotyping. Cancer Res. 59:141-150.
22. Adey A, Burton JN, Kitzman JO, Hiatt JB, Lewis AP, Martin BK, Qiu R, Lee C, Shendure J. 2013. The haplotype-resolved genome and epigenome of the aneuploid HeLa cancer cell line. Nature 500:207-211. http: //dx.doi.org/10.1038/nature12064.
23. Landry JJ, Pyl PT, Rausch T, Zichner T, Tekkedil MM, Stutz AM, Jauch A, Aiyar RS, Pau G, Delhomme N, Gagneur J, Korbel JO, Huber W, Steinmetz LM. 2013. The genomic and transcriptomic landscape of a HeLa cell line. G3 3:1213-1224. http://dx.doi.org/10.1534/g3.113.005777.
24. Heilbronn R, Bu¨rkle A, Stephan S, zur Hausen H. 1990. The adenoassociated virus rep gene suppresses herpes simplex virus-induced DNAamplification. J. Virol. 64:3012-3018.
25. Hu¨ser D, Weger S, Heilbronn R. 2003. Packaging of human chromosome 19-specific adeno-associated virus (AAV) integration sites in AAV virions during AAV wild-type and recombinant AAV vector production. J. Virol. 77:4881-4887. http://dx.doi.org/10.1128/JVI.77.8 .4881-4887.2003.
26. Mietzsch M, Grasse S, Zurawski C, Weger S, Bennett A, Agbandje-McKenna M, Muzyczka N, Zolotukhin S, Heilbronn R. 2014. OneBac: platform for scalable and high-titer production of adeno-associated virus serotype 1-12 vectors for gene therapy. Hum. Gene Ther. 25:212-222. http://dx.doi.org/10.1089/hum.2013.184.
27. Weindler FW, Heilbronn R. 1991. A subset of herpes simplex virus replication genes provides helper functions for productive adenoassociated virus replication. J. Virol. 65:2476-2483.
28. Pages H, Aboyoun P, Gentleman R, DebRoy S. 2007. Biostrings: string objects representing biological sequences, and matching algorithms. http: //bioconductor.wustl.edu/bioc/html/Biostrings.html.
29. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9:357-359. http://dx.doi.org/10.1038/nmeth.1923.
30. Needleman SB, Wunsch CD. 1970. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol. 48:443-453. http://dx.doi.org/10.1016/0022-2836(70)90057-4.
31. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. http://dx.doi.org/10.1186/gb-2009-10 -3-r25.
32. Janovitz T, Sadelain M, Falck-Pedersen E. 2014. Adeno-associated virus type 2 preferentially integrates single genome copies with defined breakpoints. Virol. J. 11:15. http://dx.doi.org/10.1186/1743-422X-11-15.
33. Berthet C, Raj K, Saudan P, Beard P. 2005. How adeno-associated virus Rep78 protein arrests cells completely in S phase. Proc. Natl. Acad. Sci. U. S. A. 102:13634-13639. http://dx.doi.org/10.1073/pnas.0504583102.
34. Costello E, Saudan P, Winocour E, Pizer L, Beard P. 1997. High mobility group chromosomal protein 1 binds to the adeno-associated virus replication protein (Rep) and promotes Rep-mediated site-specific cleavage of DNA, ATPase activity, and transcriptional repression. EMBO J. 16:5943-5954. http://dx.doi.org/10.1093/emboj/16.19.5943.
35. Consortium EP, Bernstein BE, Birney E, Dunham I, Green ED, Gunter C, Snyder M. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489:57-74. http://dx.doi.org/10 .1038/nature11247.
36. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129:823-837. http://dx.doi.org/10.1016 /j.cell.2007.05.009.
37. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, Zhao K. 2008. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 40:897-903. http://dx.doi.org/10.1038/ng.154.
38. McCarty DM, Pereira DJ, Zolotukhin I, Zhou X, Ryan JH, Muzyczka N. 1994. Identification of linear DNA sequences that specifically bind the adeno-associated virus Rep protein. J. Virol. 68:4988-4997.
39. Chiorini JA, Yang L, Safer B, Kotin RM. 1995. Determination of adenoassociated virus Rep68 and Rep78 binging sites by random sequence oligonucleotide selection. J. Virol. 69:7334-7338.
40. Lamartina S, Sporeno E, Fattori E, Toniatti C. 2000. Characteristics of the adeno-associated virus preintegration site in human chromosome 19: open chromatin conformation and transcription-competent environment. J. Virol. 74:7671-7677. http://dx.doi.org/10.1128/JVI.74.16.7671 -7677.2000.
41. Hockemeyer D, Soldner F, Beard C, Gao Q, Mitalipova M, DeKelver RC, Katibah GE, Amora R, Boydston EA, Zeitler B, Meng X, Miller JC, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Jaenisch R. 2009. Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat. Biotechnol. 27:851-857. http://dx.doi.org/10 .1038/nbt.1562.