Crystal structure of the Rous sarcoma virus intasome

Nature

Volumn 530, Issue 7590, 2016, Pages 362-366

  Yin, Zhiqi ^a,b,c   Shi, Ke ^a,b,c   Banerjee, Surajit ^d   Pandey, Krishan K ^e   Bera, Sibes ^e   Grandgenett, Duane P ^e   Aihara, Hideki ^a,b,c  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d Department of Obstetrics Gynecology   (United States)

^e SAINT LOUIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRASE; VIRUS DNA; PROTEIN BINDING;

CATALYSIS; CHROMOSOME; CRYSTAL STRUCTURE; DNA; GENOME; HUMAN IMMUNODEFICIENCY VIRUS; LIFE CYCLE ANALYSIS; MOLECULAR ANALYSIS; PROTEIN; VIRUS;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; DNA BINDING; GENE TARGETING; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; ROUS SARCOMA VIRUS; SPUMAVIRUS; VIRUS DNA CELL DNA INTERACTION; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR MODEL; PROTEIN MULTIMERIZATION; X RAY CRYSTALLOGRAPHY;

HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN SPUMARETROVIRUS; ROUS SARCOMA VIRUS;

CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DNA, VIRAL; HIV-1; INTEGRASES; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN MULTIMERIZATION; ROUS SARCOMA VIRUS; SPUMAVIRUS; VIRUS INTEGRATION;

EID: 84959019653     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature16950     Document Type: Article

References (42)

1. Craigie, R., Bushman, F. D. HIV DNA integration. Cold Spring Harb. Perspect. Med. 2, a006890 (2012).
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 mechanism of retroviral integration from X-ray structures of its key intermediates. Nature 468, 326-329 (2010).
4. Maskell, D. P. et al. Structural basis for retroviral integration into nucleosomes. Nature 523, 366-369 (2015).
5. 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).
6. Shi, K. et al. A possible role for the asymmetric C-terminal domain dimer of Rous sarcoma virus integrase in viral DNA binding. PLoS ONE 8, e56892 (2013).
7. 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).
8. Yang, Z. N., Mueser, T. C., Bushman, F. D., Hyde, C. C. Crystal structure of an active two-domain derivative of Rous sarcoma virus integrase. J. Mol. Biol. 296, 535-548 (2000).
9. Vora, A., Bera, S., Grandgenett, D. Structural organization of avian retrovirus integrase in assembled intasomes mediating full-site integration. J. Biol. Chem. 279, 18670-18678 (2004).
10. Gao, K., Butler, S. L., Bushman, F. Human immunodeficiency virus type 1 integrase: arrangement of protein domains in active cDNA complexes. EMBO J. 20, 3565-3576 (2001).
11. Peletskaya, E. et al. Localization of ASV integrase-DNA contacts by site-directed crosslinking and their structural analysis. PLoS ONE 6, e27751 (2011).
12. Lutzke, R. A., Plasterk, R. H. Structure-based mutational analysis of the C-terminal DNA-binding domain of human immunodeficiency virus type 1 integrase: critical residues for protein oligomerization and DNA binding. J. Virol. 72, 4841-4848 (1998).
13. Chiu, R., Grandgenett, D. P. Molecular and genetic determinants of rous sarcoma virus integrase for concerted DNA integration. J. Virol. 77, 6482-6492 (2003).
14. Chen, H., Wei, S. Q., Engelman, A. Multiple integrase functions are required to form the native structure of the human immunodeficiency virus type I intasome. J. Biol. Chem. 274, 17358-17364 (1999).
15. Li, M., Craigie, R. Processing of viral DNA ends channels the HIV-1 integration reaction to concerted integration. J. Biol. Chem. 280, 29334-29339 (2005).
16. Bojja, R. S. et al. Architecture of a full-length retroviral integrase monomer and dimer, revealed by small angle X-ray scattering and chemical cross-linking. J. Biol. Chem. 286, 17047-17059 (2011).
17. Lubkowski, J. et al. Atomic resolution structures of the core domain of avian sarcoma virus integrase and its D64N mutant. Biochemistry 38, 13512-13522 (1999).
18. Quashie, P. K. et al. Characterization of the R263K mutation in HIV-1 integrase that confers low-level resistance to the second-generation integrase strand transfer inhibitor dolutegravir. J. Virol. 86, 2696-2705 (2012).
19. Montanõ, S. P., Pigli, Y. Z., Rice, P. A. The Mu transpososome structure sheds light on DDE recombinase evolution. Nature 491, 413-417 (2012).
20. Harper, A. L., Sudol, M., Katzman, M. An amino acid in the central catalytic domain of three retroviral integrases that affects target site selection in nonviral DNA. J. Virol. 77, 3838-3845 (2003).
21. Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F., Richmond, T. J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251-260 (1997).
22. Serrao, E., Ballandras-Colas, A., Cherepanov, P., Maertens, G. N., Engelman, A. N. Key determinants of target DNA recognition by retroviral intasomes. Retrovirology 12, 39 (2015).
23. Wu, X., Li, Y., Crise, B., Burgess, S. M., Munroe, D. J. Weak palindromic consensus sequences are a common feature found at the integration target sites of many retroviruses. J. Virol. 79, 5211-5214 (2005).
24. Aiyer, S. et al. Structural and sequencing analysis of local target DNA recognition by MLV integrase. Nucleic Acids Res. 43, 5647-5663 (2015).
25. Ballandras-Colas, A. et al. Cryo-EM reveals a novel octameric integrase structure for ?-retrovirus intasome function. Nature http://dx.doi.org/10.1038/nature16955 (this issue).
26. Temin, H. M. The participation of DNA in Rous sarcoma virus production. Virology 23, 486-494 (1964).
27. Grandgenett, D. P., Vora, A. C., Schiff, R. D. A 32,000-dalton nucleic acid-binding protein from avian retravirus cores possesses DNA endonuclease activity. Virology 89, 119-132 (1978).
28. Donehower, L. A., Varmus, H. E. A mutant murine leukemia virus with a single missense codon in pol is defective in a function affecting integration. Proc. Natl Acad. Sci. USA 81, 6461-6465 (1984).
29. Panganiban, A. T., Temin, H. M. The retrovirus pol gene encodes a product required for DNA integration: identification of a retrovirus int locus. Proc. Natl Acad. Sci. USA 81, 7885-7889 (1984).
30. Schwartzberg, P., Colicelli, J., Goff, S. P. Construction and analysis of deletion mutations in the pol gene of Moloney murine leukemia virus: a new viral function required for productive infection. Cell 37, 1043-1052 (1984).
31. Vora, A. C. et al. Avian retrovirus U3 and U5 DNA inverted repeats. Role of nonsymmetrical nucleotides in promoting full-site integration by purified virion and bacterial recombinant integrases. J. Biol. Chem. 272, 23938-23945 (1997).
32. Otwinowski, Z., Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276, 307-326 (1997).
33. Kabsch, W. XDS. Acta Crystallogr. D 66, 125-132 (2010).
34. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
35. Vagin, A., Teplyakov, A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025 (1997).
36. Emsley, P., Lohkamp, B., Scott, W. G., Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
37. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
38. Šali, A., Blundell, T. L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815 (1993).
39. Wang, J. Y., Ling, H., Yang, W., Craigie, R. Structure of a two-domain fragment of HIV-1 integrase: implications for domain organization in the intact protein. EMBO J. 20, 7333-7343 (2001).
40. Karplus, P. A., Diederichs, K. Linking crystallographic model and data quality. Science 336, 1030-1033 (2012).
41. Robert, X., Gouet, P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 42, W320-W324 (2014).
42. Pandey, K. K. et al. Rous sarcoma virus synaptic complex capable of concerted integration is kinetically trapped by human immunodeficiency virus integrase strand transfer inhibitors. J. Biol. Chem. 289, 19648-19658 (2014).