The DOI matches its Crossref record; 46 of the 47 references it cites were found in a registry or an index.
MLV integration site selection is driven by strong enhancers and active promoters
Open accessAbstract
Retroviruses integrate into the host genome in patterns specific to each virus. Understanding the causes of these patterns can provide insight into viral integration mechanisms, pathology and genome evolution, and is critical to the development of safe gene therapy vectors. We generated murine leukemia virus integrations in human HepG2 and K562 cells and subjected them to second-generation sequencing, using a DNA barcoding technique that allowed us to quantify independent integration events. We characterized >3 700 000 unique integration events in two ENCODE-characterized cell lines. We find that integrations were most highly enriched in a subset of strong enhancers and active promoters. In both cell types, approximately half the integrations were found in <2% of the genome, demonstrating genomic influences even narrower than previously believed. The integration pattern of murine leukemia virus appears to be largely driven by regions that have high enrichment for multiple marks of active chromatin; the combination of histone marks present was sufficient to explain why some strong enhancers were more prone to integration than others. The approach we used is applicable to analyzing the integration pattern of any exogenous element and could be a valuable preclinical screen to evaluate the safety of gene therapy vectors.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“The well-understood integration preferences of HIV-1 for active transcription units72 and MLV for promoter/enhancer regions73–75 are in large part dictated via specific interactions of the respective IN proteins with chromatin-bound host factors.”
From Structure and function of retroviral integrase (2022) · cites this paper as [75]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“BET proteins significantly stimulate γ-retroviral IN strand transfer activities in vitro67,115,116 and appear to act as bimodal tethers to direct PICs to preferred genomic locations74,75,114,117,118.”
From Structure and function of retroviral integrase (2022) · cites this paper as [75]
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
R: A Language and Environment for Statistical Computing
R Core Team (2000) · doi:10.32614/r.manuals · Cited by 355,893
Cutadapt removes adapter sequences from high-throughput sequencing reads
Martin, M. (2011) · EMBnet.journal · doi:10.14806/ej.17.1.200 · Cited by 33,889
BEDTools: a flexible suite of utilities for comparing genomic features
Quinlan, A. R., & Hall, I. M. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq033 · Cited by 27,437
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849
An integrated encyclopedia of DNA elements in the human genome
The ENCODE Project Consortium (2012) · Nature · doi:10.1038/nature11247 · Cited by 18,072
ggplot2: Elegant Graphics for Data Analysis
Wickham, H. (2009) · doi:10.1007/978-0-387-98141-3 · Cited by 14,447
The Human Genome Browser at UCSC
Kent, W. J., Sugnet, C. W., Furey, T. S., Roskin, K. M., Pringle, T. H., Zahler, A. M., & Haussler, A. D. (2002) · Genome Research · doi:10.1101/gr.229102 · Cited by 10,400
Genome-wide maps of chromatin state in pluripotent and lineage-committed cells
Mikkelsen, T. S., Ku, M., Jaffe, D. B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T.-K., Koche, R. P., et al. (2007) · Nature · doi:10.1038/nature06008 · Cited by 4,129
Mapping and analysis of chromatin state dynamics in nine human cell types
Ernst, J., Kheradpour, P., Mikkelsen, T. S., Shoresh, N., Ward, L. D., Epstein, C. B., Zhang, X., Wang, L., Issner, R., Coyne, M., et al. (2011) · Nature · doi:10.1038/nature09906 · Cited by 2,898
Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1
Hacein-Bey-Abina, S., Garrigue, A., Wang, G. P., Soulier, J., Lim, A., Morillon, E., Clappier, E., Caccavelli, L., Delabesse, E., Beldjord, K., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci35700 · Cited by 1,854
Flagged first, then by citations
1 of the 47 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- Coffin, 1997, Retroviruses
Cited by
Sorted by citations
Vector design influences hepatic genotoxicity after adeno-associated virus gene therapy
Chandler, R. J., LaFave, M. C., Varshney, G. K., Trivedi, N. S., Carrillo-Carrasco, N., Senac, J. S., Wu, W., Hoffmann, V., Elkahloun, A. G., Burgess, S. M., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci79213 · Cited by 403
Self-citationIntegration site selection by retroviruses and transposable elements in eukaryotes
Sultana, T., Zamborlini, A., Cristofari, G., & Lesage, P. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2017.7 · Cited by 275
Lesbats, P., Engelman, A., & Cherepanov, P. (2016) · Chemical Reviews · doi:10.1021/acs.chemrev.6b00125 · Cited by 250
Progresses towards safe and efficient gene therapy vectors
Chira, S., Jackson, C. S., Oprea, I. I., Öztürk, F., Pepper, M. S., Diaconu, I., Braicu, C., Ráduly, L., Călin, G. A., & Berindan‐Neagoe, I. (2015) · Oncotarget · doi:10.18632/oncotarget.5169 · Cited by 227
Viral Vectors: The Road to Reducing Genotoxicity
David, R. M., & Doherty, A. (2016) · Toxicological Sciences · doi:10.1093/toxsci/kfw220 · Cited by 176
Gogol‐Döring, A., Ammar, I., Gupta, S., Bunse, M., Miskey, C., Chen, W., Uckert, W., Schulz, T. F., Izsvák, Z., & Ivics, Z. (2016) · Molecular Therapy · doi:10.1038/mt.2016.11 · Cited by 165
Shah, N. N., Qin, H., Yates, B., Su, L., Shalabi, H., Raffeld, M. A., Ahlman, M. A., Stetler‐Stevenson, M., Yuan, C. M., Guo, S., et al. (2019) · Blood Advances · doi:10.1182/bloodadvances.2019000219 · Cited by 162
Sultana, T., van Essen, D., Siol, O., Bailly-Bechet, M., Philippe, C., Zine El Aabidine, A., Pioger, L., Nigumann, P., Saccani, S., Andrau, J.-C., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.02.036 · Cited by 154
Molecular mechanisms of retroviral integration site selection
Kvaratskhelia, M., Sharma, A., Larue, R. C., Serrao, E., & Engelman, A. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku769 · Cited by 150
Burrows, C. K., Banovich, N. E., Pavlovic, B. J., Patterson, K. M., Romero, I. G., Pritchard, J. K., & Gilad, Y. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1005793 · Cited by 136
Structure and function of retroviral integrase
Maertens, G. N., Engelman, A. N., & Cherepanov, P. (2022) · Nature Reviews Microbiology · doi:10.1038/s41579-021-00586-9 · Cited by 124
Genome-wide de novo L1 Retrotransposition Connects Endonuclease Activity with Replication
Flasch, D. A., Macia, Á., Sánchez, L., Ljungman, M., Heras, S. R., García-Pérez, J. L., Wilson, T. E., & Moran, J. V. (2019) · Cell · doi:10.1016/j.cell.2019.02.050 · Cited by 127
LEDGF/p75 interacts with mRNA splicing factors and targets HIV-1 integration to highly spliced genes
Singh, P. K., Plumb, M. R., Ferris, A. L., Iben, J. R., Wu, X., Fadel, H. J., Luke, B. T., Esnault, C., Poeschla, E. M., Hughes, S. H., et al. (2015) · Genes & Development · doi:10.1101/gad.267609.115 · Cited by 109
Spatially clustered loci with multiple enhancers are frequent targets of HIV-1 integration
Lucic, B., Chen, H., Kuzman, M., Zorita, E. V., Wegner, J., Minneker, V., Wang, W., Fronza, R., Laufs, S., Schmidt, M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12046-3 · Cited by 111
Understanding and Editing the Zebrafish Genome
Varshney, G. K., Sood, R. B., & Burgess, S. M. (2015) · Advances in genetics · doi:10.1016/bs.adgen.2015.09.002 · Cited by 103
Self-citationCellular and molecular mechanisms of HIV-1 integration targeting
Engelman, A., & Singh, P. K. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2772-5 · Cited by 102
Long-Term Correction of Sandhoff Disease Following Intravenous Delivery of rAAV9 to Mouse Neonates
Walia, J. S., Altaleb, N., Bello, A., Kruck, C., LaFave, M. C., Varshney, G. K., Burgess, S. M., Chowdhury, B., Hurlbut, D. J., Hemming, R., et al. (2014) · Molecular Therapy · doi:10.1038/mt.2014.240 · Cited by 93
Self-citationINSPIIRED: Quantification and Visualization Tools for Analyzing Integration Site Distributions
Berry, C. C., Nobles, C. L., Six, E. M., Wu, Y., Malani, N., Sherman, E. A., Dryga, A., Everett, J. K., Male, F., Bailey, A., et al. (2016) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2016.11.003 · Cited by 89
Crowe, B. L., Larue, R. C., Yuan, C., Hess, S., Kvaratskhelia, M., & Foster, M. P. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1516813113 · Cited by 83
Demeulemeester, J., De Rijck, J., Gijsbers, R., & Debyser, Z. (2015) · BioEssays · doi:10.1002/bies.201500051 · Cited by 71
What Integration Sites Tell Us about HIV Persistence
Hughes, S. H., & Coffin, J. M. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.04.010 · Cited by 74
Li, W., Singh, P. K., Sowd, G. A., Bedwell, G. J., Jang, S., Achuthan, V., Oleru, A. V., Wong, D., Fadel, H. J., Lee, K., et al. (2020) · mBio · doi:10.1128/mbio.02254-20 · Cited by 64
Key determinants of target DNA recognition by retroviral intasomes
Serrao, E., Ballandras-Colas, A., Cherepanov, P., Maertens, G. N., & Engelman, A. N. (2015) · Retrovirology · doi:10.1186/s12977-015-0167-3 · Cited by 62
Ninova, M., Godneeva, B. K., Chen, Y.-C. A., Luo, Y., Prakash, S. J., Jankovics, F., Erdélyi, M., Aravin, A. A., & Tóth, K. F. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.09.033 · Cited by 59
Yoshida, J., Akagi, K., Misawa, R., Kokubu, C., Takeda, J., & Horie, K. (2017) · Scientific Reports · doi:10.1038/srep43613 · Cited by 62
Shao, L., Shi, R., Zhao, Y., Liu, H., Lu, A., Ma, J., Cai, Y., Fuksenko, T., Pelayo, A., Shah, N. N., et al. (2022) · Journal of Translational Medicine · doi:10.1186/s12967-022-03729-5 · Cited by 56
Amplification, Next-generation Sequencing, and Genomic DNA Mapping of Retroviral Integration Sites
Serrao, E., Cherepanov, P., & Engelman, A. (2016) · Journal of Visualized Experiments · doi:10.3791/53840 · Cited by 63
Structural basis for spumavirus GAG tethering to chromatin
Lesbats, P., Serrao, E., Maskell, D. P., Pye, V. E., O’Reilly, N., Lindemann, D., Engelman, A. N., & Cherepanov, P. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1621159114 · Cited by 51
BET-independent MLV-based Vectors Target Away From Promoters and Regulatory Elements
Ashkar, S. E., Rijck, J. D., Demeulemeester, J., Vets, S., Madlala, P., Čermáková, K., Debyser, Z., & Gijsbers, R. (2014) · Molecular Therapy — Nucleic Acids · doi:10.1038/mtna.2014.33 · Cited by 50
Wang, W., Fasolino, M., Cattau, B., Goldman, N., Kong, W., Frederick, M. A., McCright, S. J., Kiani, K., Fraietta, J. A., & Vahedi, G. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1919259117 · Cited by 47
Shao, W., Shan, J., Kearney, M. F., Wu, X., Maldarelli, F. M., Mellors, J. W., Luke, B. T., Coffin, J. M., & Hughes, S. H. (2016) · Retrovirology · doi:10.1186/s12977-016-0277-6 · Cited by 45
Wells, D., Guo, S., Shao, W., Bale, M. J., Coffin, J. M., Hughes, S. H., & Wu, X. (2020) · BMC Genomics · doi:10.1186/s12864-020-6647-4 · Cited by 46
Wolff, J. H., & Mikkelsen, J. G. (2022) · Journal of Biomedical Science · doi:10.1186/s12929-022-00865-4 · Cited by 47
Aiyer, S., Swapna, G. V. T., Ma, L.-C., Liu, G., Hao, J., Chalmers, G., Jacobs, B. C., Montelione, G. T., & Roth, M. J. (2021) · Structure · doi:10.1016/j.str.2021.01.010 · Cited by 35
Strategies for Targeting Retroviral Integration for Safer Gene Therapy: Advances and Challenges
Yoder, K. E., Rabe, A. J., Fishel, R. A., & Larue, R. C. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.662331 · Cited by 37
Hogan, D. J., Zhu, J., Diago, O. R., Gammon, D., Haghighi, A., Lu, G., Das, A., Gruber, H. E., Jolly, D. J., & Ostertag, D. G. (2018) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-18-0619 · Cited by 33
Naughtin, M., Haftek-Terreau, Z., Xavier, J., Meyer, S., Silvain, M., Jaszczyszyn, Y., Levy, N., Miele, V., Benleulmi, M. S., Ruff, M., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129427 · Cited by 34
Advances in high-throughput methods for the identification of virus receptors
Barrass, S. V., & Butcher, S. J. (2019) · Medical Microbiology and Immunology · doi:10.1007/s00430-019-00653-2 · Cited by 30
Sites of retroviral DNA integration: From basic research to clinical applications
Serrao, E., & Engelman, A. (2015) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2015.1102859 · Cited by 32
Common Viral Integration Sites Identified in Avian Leukosis Virus-Induced B-Cell Lymphomas
Justice, J., Morgan, R. W., & BEEMON, K. L. (2015) · mBio · doi:10.1128/mbio.01863-15 · Cited by 27
Ciuffi, A. (2016) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2016.02.013 · Cited by 27
Clinical and Translational Landscape of Viral Gene Therapies
Yudaeva, A., Kostyusheva, A., Kachanov, A., Brezgin, S., Ponomareva, N., Parodi, A., Pokrovsky, V. S., Lukashev, A. N., Chulanov, V., & Kostyushev, D. S. (2024) · Cells · doi:10.3390/cells13221916 · Cited by 30
Hotspots of MLV integration in the hematopoietic tumor genome
Tsuruyama, T., Hiratsuka, T., & Yamada, N. (2016) · Oncogene · doi:10.1038/onc.2016.285 · Cited by 26
Structural and sequencing analysis of local target DNA recognition by MLV integrase
Aiyer, S., Rossi, P., Malani, N., Schneider, W. M., Chandar, A., Bushman, F. D., Montelione, G. T., & Roth, M. J. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv410 · Cited by 25
Sokol, M., Wabl, M. R., Ruiz, I. R., & Pedersen, F. S. (2014) · Retrovirology · doi:10.1186/1742-4690-11-36 · Cited by 25
Vranckx, L. S., Demeulemeester, J., Debyser, Z., & Gijsbers, R. (2016) · PLoS ONE · doi:10.1371/journal.pone.0164167 · Cited by 24
Epigenetic and chromosomal features drive transposon insertion inDrosophila melanogaster
Cao, J., Yu, T., Xu, B., Hu, Z., Zhang, X.-O., Theurkauf, W. E., & Weng, Z. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad054 · Cited by 22
Hunting Viral Receptors Using Haploid Cells
Pillay, S., & Carette, J. E. (2015) · Annual Review of Virology · doi:10.1146/annurev-virology-100114-055119 · Cited by 23
Cui, P., Löber, U., Alquezar‐Planas, D. E., Ishida, Y., Courtiol, A., Timms, P., Johnson, R. N., Lenz, D., Helgen, K. M., Roca, A. L., et al. (2016) · PeerJ · doi:10.7717/peerj.1847 · Cited by 20
Vrljicak, P., Tao, S., Varshney, G. K., Quach, H. N. B., Joshi, A., LaFave, M. C., Burgess, S. M., & Sampath, K. (2016) · G3 Genes Genomes Genetics · doi:10.1534/g3.115.026849 · Cited by 19
Self-citationIntegration Site and Clonal Expansion in Human Chronic Retroviral Infection and Gene Therapy
Niederer, H. A., & Bangham, C. R. M. (2014) · Viruses · doi:10.3390/v6114140 · Cited by 23
A Multifunctional Mutagenesis System for Analysis of Gene Function in Zebrafish
Quach, H. N. B., Tao, S., Vrljicak, P., Joshi, A., Ruan, H., Sukumaran, R., Varshney, G. K., LaFave, M. C., The Ds Screen Team, Burgess, S. M., et al. (2015) · G3 Genes Genomes Genetics · doi:10.1534/g3.114.015842 · Cited by 17
Self-citationKitawi, R. C., Ledger, S., Kelleher, A. D., & Ahlenstiel, C. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25052771 · Cited by 18
HIV-1 Integrates Widely throughout the Genome of the Human Blood Fluke Schistosoma mansoni
Suttiprapa, S., Rinaldi, G., Tsai, I. J., Mann, V. H., Dubrovsky, L., Yan, H.-B., Holroyd, N. E., Huckvale, T., Durrant, C., Protasio, A. V., et al. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005931 · Cited by 18
Seiler, C., Gebhart, N., Zhang, Y., Shinton, S. A., Li, Y., Ross, N. L., Liu, X., Li, Q., Bilbee, A. N., Varshney, G. K., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0131908 · Cited by 17
Self-citationFunctional therapies for cutaneous wound repair in epidermolysis bullosa
Peking, P., Koller, U., & Murauer, E. M. (2017) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2017.12.003 · Cited by 16
Herbst, F., Lang, T. J. L., Eckert, E., Wünsche, P., Wurm, A. A., Kindinger, T., Laaber, K., Hemmati, S., Hotz‐Wagenblatt, A., Zavidij, O., et al. (2021) · Leukemia · doi:10.1038/s41375-021-01267-5 · Cited by 14
The RUNX Genes as Conditional Oncogenes: Insights from Retroviral Targeting and Mouse Models
Neil, J. C., Gilroy, K. L., Borland, G., Hay, J., Terry, A., & Kilbey, A. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-3233-2_16 · Cited by 15
Mapping Active Gene-Regulatory Regions in Human Repopulating Long-Term HSCs
Wünsche, P., Eckert, E., Holland‐Letz, T., Paruzynski, A., Hotz‐Wagenblatt, A., Fronza, R., Rath, T., Gil-Fariña, I., Schmidt, M., Kalle, C. V., et al. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.06.003 · Cited by 14
Loyola, L. M., Achuthan, V., Gilroy, K. L., Borland, G., Kilbey, A., Mackay, N. A., Bell, M., Hay, J., Aiyer, S., Fingerman, D., et al. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1008154 · Cited by 14
Miklík, D., Šenigl, F., & Hejnar, J. (2018) · Viruses · doi:10.3390/v10030116 · Cited by 13
Virus–Host Interactions in Retrovirus Integration
Engelman, A. N., & Maertens, G. N. (2018) · Retrovirus-Cell Interactions · doi:10.1016/b978-0-12-811185-7.00004-2 · Cited by 12
Gallay, K., Blot, G., Chahpazoff, M., Yajjou, H., Confort, M.-P., de Boisséson, C., Roux, A. L., Luengo, C., Fiorini, F., Lavigne, M., et al. (2019) · Virology · doi:10.1016/j.virol.2019.04.002 · Cited by 10
Pellaers, E., Bhat, A., Christ, F., & Debyser, Z. (2022) · Viruses · doi:10.3390/v15010032 · Cited by 8
Gene therapy strategies for RAG1 deficiency: Challenges and breakthroughs
Gilioli, G., Lankester, A. C., de Kivit, S., Staal, F. J. T., & de Bruin, L. M. O. (2024) · Immunology Letters · doi:10.1016/j.imlet.2024.106931 · Cited by 8
GeIST: a pipeline for mapping integrated DNA elements
LaFave, M. C., Varshney, G. K., & Burgess, S. M. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv350 · Cited by 8
Self-citationGilroy, K. L., Terry, A., Naseer, A., de Ridder, J., Allahyar, A., Wang, W., Carpenter, E. J., Mason, A. L., Wong, G. K., Cameron, E. R., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0154070 · Cited by 8
Šenigl, F., Miklík, D., Auxt, M., & Hejnar, J. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx889 · Cited by 7
Improved functionality and potency of next generation BinMLV viral vectors toward safer gene therapy
Looveren, D. V., Giacomazzi, G., Thiry, I., Sampaolesi, M., & Gijsbers, R. (2021) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2021.07.003 · Cited by 7
Nombela, I., Michiels, M., Looveren, D. V., Marcelis, L., Ashkar, S. E., Belle, S. V., Bruggemans, A., Tousseyn, T., Schwaller, J., Christ, F., et al. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.01478-22 · Cited by 7
Applications of DNA integrating elements: Facing the bias bully
de Jong, J., Wessels, L. F. A., van Lohuizen, M., de Ridder, J., & Akhtar, W. (2014) · Mobile Genetic Elements · doi:10.4161/2159256x.2014.992694 · Cited by 8
Akkawi, C., Feuillard, J., Leon-Diaz, F., Belkhir, K., Godefroy, N., Péloponèse, J., Mougel, M., & Lainé, S. (2023) · Retrovirology · doi:10.1186/s12977-023-00631-w · Cited by 6
Evolution of a Restriction Factor by Domestication of a Yeast Retrotransposon
Hannon-Hatfield, J. A., Chen, J., Bergman, C., & Garfinkel, D. J. (2024) · Molecular Biology and Evolution · doi:10.1093/molbev/msae050 · Cited by 6
Contrasting segregation patterns among endogenous retroviruses across the koala population
Lillie, M., Pettersson, M. E., & Jern, P. (2024) · Communications Biology · doi:10.1038/s42003-024-06049-0 · Cited by 8
Nam, J.-S., Lee, J.-E., Lee, K.-H., Yang, Y., Kim, S.-H., Bae, G., Noh, H., & Lim, K. (2018) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2018.11.001 · Cited by 5
Pathogenetic Therapy of Epidermolysis Bullosa: Current State and Prospects
Ryumina, I. I., Goryunov, K. V., Silachev, D. N., Shevtsova, Y. А., Babenko, V. А., Михайловна, М. Н., Kotalevskaya, Y. Y., Zubkov, V. V., & Zubkov, G. T. (2021) · Bulletin of Experimental Biology and Medicine · doi:10.1007/s10517-021-05182-8 · Cited by 5
Miklík, D., Grim, J., Elleder, D., & Hejnar, J. (2023) · Genome Research · doi:10.1101/gr.277694.123 · Cited by 4
The role of chromatin in retroviral preintegration complex function
Sapp, N., Prakash, P., Chakraborty, R., Balasubramaniam, M., & Dash, C. (2025) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2025.110440 · Cited by 3
Liu, Q., Wang, X., Du, C., Lin, Y., Ma, J., Wang, Y., Zhou, J.-H., & Wang, X. (2017) · Journal of General Virology · doi:10.1099/jgv.0.000918 · Cited by 3
Webster, P., Dawes, J., Dewchand, H., Takács, K., Iadarola, B., Bolt, B. J., Cáceres, J. J., Kaczor, J., Dharmalingam, G., Dore, M. H., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05069-9 · Cited by 3
Comparing the landcapes of common retroviral insertion sites across tumor models
Weishaupt, H., Čančer, M., Engström, C., Silvestrov, S. D., & Swartling, F. J. (2017) · AIP conference proceedings · doi:10.1063/1.4972765 · Cited by 2
Le rôle des protéines BET dans l’intégration des γ-rétrovirus
Albagli, O., & Pelczar, H. (2016) · médecine/sciences · doi:10.1051/medsci/20163212009 · Cited by 2
Long Terminal Repeats of Gammaretroviruses Retain Stable Expression after Integration Retargeting
Miklík, D., Slavková, M., Kučerová, D., Mekadim, C., Mrázek, J., & Hejnar, J. (2024) · Viruses · doi:10.3390/v16101518 · Cited by 2
PRISM-Seq: An Ultra-sensitive Sequencing Approach For Mapping Lentiviral Integration SitesPreprint
Pal, V. K., Canis, M., Stone, E., Nathan L. Board, Lenart, K., Fumagalli, M. J., Kovas, C., Jones, R. B., Nussenzweig, M. C., Muecksch, F., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.20.695659 · Cited by 2
Fetal Hemoglobin Research and Clinical Relevance in Sickle Cell Disease
Gudmundsdóttir, B. K., & Tisdale, J. F. (2025) · Physiology · doi:10.1152/physiol.00024.2025 · Cited by 1
Basic Research and Clinical Examination of Tumor Virus
Tsuruyama, T., Ogawa, S., & Yamada, N. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.89331 · Cited by 1
Transcriptional Control and Latency of Retroviruses
Nikolai, B. C., & Rice, A. P. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-811185-7.00005-4 · Cited by 1
Yang, Y., Lee, J., Jeong, H., Shim, J., Baek, M., Son, M.-J., Kim, Y., Noh, H., & Lim, K. (2020) · Biotechnology and Bioengineering · doi:10.1002/bit.27540 · Cited by 1
Retroviral Vectors for Gene Therapy of Monogenic Diseases
Yoder, K. E., Rabe, A. J., & Larue, R. C. (2022) · Springer eBooks · doi:10.1007/978-3-030-93333-3_7 · Cited by 1
Neil, J. C. (2017) · Wiley eBooks · doi:10.1002/9780470015902.a0024847 · Cited by 1
Freitas, E. H. D. S., de Noronha, S. M. R., Ritto, M. D. N. G., Baptista, C. F., da Silva, I. D. C. G., Correa-Noronha, S. A. A., & Silva, I. (2014) · American Journal of Molecular Biology · doi:10.4236/ajmb.2014.44020
SURVEY AND SUMMARY Molecular mechanisms of retroviral integration site selection
Kvaratskhelia, M., Sharma, A., Larue, R. C., Serrao, E., & Engelman, A. (2014)
Treating Hemophilia by Gene Therapy
Porada, C. D., Ignacio, G., Atala, A., & Almeida-Porada, G. D. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-800548-4.00012-7
Retroviral Scanning: Mapping MLV Integration Sites to Define Cell-specific Regulatory Regions
Romano, O., Cifola, I., Poletti, V., Severgnini, M., Peano, C., Bellis, G. D., Mavilio, F., & Miccio, A. (2017) · Journal of Visualized Experiments · doi:10.3791/55919
Enhort: a platform for deep analysis of genomic positions
Menzel, M., Koch, P., Glasenhardt, S., & Gogol‐Döring, A. (2019) · PeerJ Computer Science · doi:10.7717/peerj-cs.198
Peer Review #1 of "Enhort: a platform for deep analysis of genomic positions (v0.1)"
(2019) · PeerJ Computer Science · doi:10.7287/peerj-cs.198v0.1/reviews/1
Shimode, S., & Yamamoto, T. (2021) · Virus Genes · doi:10.1007/s11262-021-01878-1
Nombela, I., Michiels, M., Looveren, D. V., Marcelis, L., Ashkar, S. E., Belle, S. V., Bruggemans, A., Tousseyn, T., Schwaller, J., Christ, F., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.02.23.481640
Peer Review #2 of "Enhort: a platform for deep analysis of genomic positions (v0.2)"
(2019) · PeerJ Computer Science · doi:10.7287/peerj-cs.198v0.2/reviews/2
Zhang, H., Yang, L., Xu, J., & Yen, K. (2021) · Scientia Sinica Vitae · doi:10.1360/ssv-2021-0118
Metadata
- Authors
- LaFave, M. C., Varshney, G. K., Gildea, D. E., Wolfsberg, T. G., Baxevanis, A. D., & Burgess, S. M.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Burgess, Shawn M.
- ORCID
- Venue
- Nucleic Acids Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-01-23
- Volume
- 42
- Issue
- 7
- Pages
- 4257-4269
- ISSN
- 0305-1048 (ISSN-L)
- 1362-4962
- PMC
- PMC3985626
- OpenAlex
- W2034118113
- Cited by
- 114
- References
- 47
- Citations by year
- 2025: 3 · 2024: 8 · 2023: 8 · 2022: 6 · 2021: 8 · 2020: 5 · 2019: 14 · 2018: 9 · 2017: 10 · 2016: 20 · 2015: 15 · 2014: 8
- FWCI
- 11.46
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- public-domain
- Locations
- Nucleic Acids Research (publishedVersion, public-domain)
- Europe PMC (PubMed Central) (publishedVersion, public-domain)
- PubMed Central (publishedVersion, public-domain)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Human Genome Research Institute
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
- Keywords
- murine leukemia virus, retroviral integration, integration site selection, enhancers, histone modifications, active chromatin, DNA barcoding, HepG2 cells, K562 cells, integration hotspots
- MeSH terms
- Attachment Sites, Microbiological, Enhancer Elements, Genetic, Humans, Moloney murine leukemia virus, Promoter Regions, Genetic, Virus Integration, K562 Cells, Cell Line, Tumor
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review