Structural basis for retroviral integration into nucleosomes

Nature

Volumn 523, Issue 7560, 2015, Pages 366-369

  Maskell, Daniel P ^a   Renault, Ludovic ^a,b   Serrao, Erik ^b   Lesbats, Paul ^a   Matadeen, Rishi ^d   Hare, Stephen ^e   Lindemann, Dirk ^f   Engelman, Alan N ^c   Costa, Alessandro ^a   Cherepanov, Peter ^a,e  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d LEIDEN UNIVERSITY   (Netherlands)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HETERODIMER; VIRUS DNA; DNA; HISTONE; INTEGRASE; NUCLEOSOME;

AMINO ACID; CHROMOSOME; DNA; ENZYME; EUKARYOTE; GENOME; PHENOTYPIC PLASTICITY; RECOMBINATION; VIRUS;

ARTICLE; CRYOELECTRON MICROSCOPY; IN VITRO STUDY; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTOTYPE FOAMY VIRUS; SPUMAVIRUS; VIRUS GENOME; AMINO ACID SUBSTITUTION; BINDING SITE; CHEMISTRY; GENETIC RECOMBINATION; GENETICS; GENOME; METABOLISM; MOLECULAR MODEL; PROTEIN MULTIMERIZATION; ULTRASTRUCTURE; VIROLOGY; VIRUS DNA CELL DNA INTERACTION;

HUMAN SPUMARETROVIRUS;

AMINO ACID SUBSTITUTION; BINDING SITES; CRYOELECTRON MICROSCOPY; DNA; GENOME; HISTONES; INTEGRASES; MODELS, MOLECULAR; NUCLEOSOMES; PROTEIN MULTIMERIZATION; RECOMBINATION, GENETIC; SPUMAVIRUS; VIRUS INTEGRATION;

EID: 84928916966     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14495     Document Type: Article

References (49)

1. Li, M., Mizuuchi, M., Burke, T. R. Jr & Craigie, R. Retroviral DNA integration: reaction pathway and critical intermediates. EMBO J. 25, 1295-1304 (2006).
2. Hare, S., Gupta, S. S., Valkov, E., Engelman, A. & Cherepanov, P. Retroviral intasome assembly and inhibition of DNA strand transfer. Nature 464, 232-236 (2010).
3. Maertens, G. N., Hare, S. & Cherepanov, P. The mechanismofretroviral integration from X-ray structures of its key intermediates. Nature 468, 326-329 (2010).
4. Montaño, S.P., Pigli, Y. Z. & Rice, P. A. The mu transpososome structure sheds light on DDE recombinase evolution. Nature 491, 413-417 (2012).
5. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F. & Richmond, T. J. Crystal structureofthe nucleosomecore particleat 2.8 Aresolution. Nature 389, 251-260(1997).
6. Pryciak, P. M., Sil, A. & Varmus, H. E. Retroviral integration into minichromosomes in vitro. EMBO J. 11, 291-303 (1992).
7. Pryciak, P. M. & Varmus, H. E. Nucleosomes, DNA-binding proteins, and DNA sequence modulate retroviral integration target site selection. Cell 69, 769-780 (1992).
8. Pruss, D., Bushman, F.D. & Wolffe, A.P. Human immunodeficiency virus integrase directs integration to sites of severe DNA distortion within the nucleosome core. Proc. Natl Acad. Sci. USA 91, 5913-5917 (1994).
9. Müller, H. P. & Varmus, H. E. DNA bending creates favored sites for retroviral integration: an explanation for preferred insertion sites in nucleosomes. EMBO J. 13, 4704-4714 (1994).
10. 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. 17, 1186-1194 (2007).
11. Roth, S. L., Malani, N. & Bushman, F. D. Gammaretroviral integration into nucleosomal target DNA in vivo. J. Virol. 85, 7393-7401 (2011).
12. Baller, J. A., Gao, J., Stamenova, R., Curcio, M. J. & Voytas, D. F. A nucleosomal surface defines an integration hotspot for the Saccharomyces cerevisiae Ty1 retrotransposon. Genome Res. 22, 704-713 (2012).
13. Hare, S., Maertens, G. N. & Cherepanov, P. 39-processing and strand transfer catalysed by retroviral integrase in crystallo. EMBO J. 31, 3020-3028 (2012).
14. Yin, Z., Lapkouski, M., Yang, W. & Craigie, R. Assembly of prototype foamy virus strand transfer complexes on product DNA bypassing catalysis of integration. Protein Sci. 21, 1849-1857 (2012).
15. Lowary, P. T. & Widom, J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276, 19-42 (1998).
16. Davey, C. A., Sargent, D. F., Luger, K., Maeder, A. W. & Richmond, T. J. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 A resolution. J. Mol. Biol. 319, 1097-1113 (2002).
17. Dyda, F.et al. Crystal structureofthe catalytic domainofHIV-1 integrase: similarity to other polynucleotidyl transferases. Science 266, 1981-1986 (1994).
18. Shaytan, A. K., Landsman, D. & Panchenko, A. R. Nucleosome adaptability conferredbysequence andstructural variationsinhistoneH2A-H2Bdimers. Curr. Opin. Struct. Biol. 32, 48-57 (2015).
19. Müllers, E. et al. Novel functionsofprototype foamy virus Gag glycine-arginine-rich boxes in reverse transcription and particle morphogenesis. J. Virol. 85, 1452-1463 (2011).
20. Trobridge, G. D. et al. Foamy virus vector integration sites in normal human cells. Proc. Natl Acad. Sci. USA 103, 1498-1503 (2006).
21. Nowrouzi, A. et al. Genome-wide mapping offoamy virus vector integrations into a human cell line. J. Gen. Virol. 87, 1339-1347 (2006).
22. Guelen, L. et al. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453, 948-951 (2008).
23. Deal, R. B., Henikoff, J. G. & Henikoff, S. Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328, 1161-1164 (2010).
24. Schwabish, M.A. & Struhl, K. Asf1 mediateshistone eviction anddeposition during elongation by RNA polymerase II. Mol. Cell 22, 415-422 (2006).
25. Gupta, K. et al. Solution conformations of prototype foamy virus integrase and its stable synaptic complex with U5 viral DNA. Structure 20, 1918-1928 (2012).
26. Valkov, E. et al. Functional and structural characterization of the integrase from the prototype foamy virus. Nucleic Acids Res. 37, 243-255 (2009).
27. Hare, S. et al. Molecular mechanisms of retroviral integrase inhibition and the evolutionofviral resistance. Proc. Natl Acad. Sci. USA 107, 20057-20062 (2010).
28. Schnitzler, G. R. Isolation of histones and nucleosome cores from mammalian cells. Curr. Protoc. Mol. Biol. Chapter 21, Unit 21 (2001).
29. Dyer, P. N. et al. Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol. 375, 23-44 (2004).
30. Mindell, J.A. & Grigorieff, N. Accurate determinationoflocal defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
31. Heymann, J. B. & Belnap, D. M. Bsoft: image processing and molecular modeling for electron microscopy. J. Struct. Biol. 157, 3-18 (2007).
32. van Heel, M., Harauz, G., Orlova, E. V., Schmidt, R. & Schatz, M. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116, 17-24 (1996).
33. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
34. Hohn, M. et al. SPARX, a new environment for Cryo-EM image processing. J. Struct. Biol. 157, 47-55 (2007).
35. de la Rosa-Trevín, J. M. et al. Xmipp 3.0: an improved software suite for image processing in electron microscopy. J. Struct. Biol. 184, 321-328 (2013).
36. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
37. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
38. Heinkelein, M. et al. Improved primate foamy virus vectors and packaging constructs. J. Virol. 76, 3774-3783 (2002).
39. Stirnnagel, K. et al. Differential pH-dependent cellular uptake pathways among foamy viruses elucidated using dual-colored fluorescent particles. Retrovirology 9, 71 (2012).
40. Stange, A., Luftenegger, D., Reh, J., Weissenhorn, W. & Lindemann, D. Subviral particle release determinants of prototype foamy virus. J. Virol. 82, 9858-9869 (2008).
41. Rasheed, S., Nelson-Rees, W. A., Toth, E. M., Arnstein, P. & Gardner, M. B. Characterization of a newly derived human sarcoma cell line (HT-1080). Cancer 33, 1027-1033 (1974).
42. Matreyek, K. A. et al. Host and viral determinants for MxB restriction of HIV-1 infection. Retrovirology 11, 90 (2014).
43. Chatterjee, A. G. et al. Serial number tagging reveals a prominent sequence preference of retrotransposon integration. Nucleic Acids Res. 42, 8449-8460 (2014).
44. Schröder, A. R. et al. HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110, 521-529 (2002).
45. Kent, W. J. BLAT-the BLAST-like alignment tool. Genome Res. 12, 656-664 (2002).
46. Deyle, D.R. et al. Agenome-wide mapofadeno-associated virus-mediated human gene targeting. Nature Struct. Mol. Biol. 21, 969-975 (2014).
47. Meuleman, W. et al. Constitutive nuclear lamina-genome interactions are highly conserved and associated with A/T-rich sequence. Genome Res. 23, 270-280 (2013).
48. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842 (2010).
49. Crooks, G.E., Hon, G., Chandonia, J. M. & Brenner, S. E. WebLogo: asequence logo generator. Genome Res. 14, 1188-1190 (2004).