A Possible Role for the Asymmetric C-Terminal Domain Dimer of Rous Sarcoma Virus Integrase in Viral DNA Binding

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Shi, Ke ^a   Pandey, Krishan K ^b   Bera, Sibes ^b   Vora, Ajaykumar C ^b   Grandgenett, Duane P ^b   Aihara, Hideki ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b SAINT LOUIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; INTEGRASE; VIRUS DNA;

AMINO TERMINAL SEQUENCE; ARTICLE; ASYMMETRIC CATALYSIS; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DIMERIZATION; DNA BINDING; DNA CROSS LINKING; GENE MUTATION; GENE TARGETING; IN VITRO STUDY; MOLECULAR DYNAMICS; MOLECULAR MODEL; MUTATIONAL ANALYSIS; NONHUMAN; ROUS SARCOMA ONCOVIRUS; VIRUS DNA CELL DNA INTERACTION; VIRUS GENOME;

DNA, VIRAL; INTEGRASES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; ROUS SARCOMA VIRUS; VIRAL PROTEINS;

EID: 84874319884     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056892     Document Type: Article

References (51)

1. Valkov E, Gupta SS, Hare S, Helander A, Roversi P, et al. (2009) Functional and structural characterization of the integrase from the prototype foamy virus. Nucleic Acids Res 37: 243-255.
2. Craigie R (2002) Retroviral DNA Integration. In: Craig NL, Craigie R, Gellert M, Lambowitz AM, editors. Mobile DNA II. Washington, DC: ASM Press. 613-630.
3. Li X, Krishnan L, Cherepanov P, Engelman A, (2011) Structural biology of retroviral DNA integration. Virology 411: 194-205.
4. Faure A, Calmels C, Desjobert C, Castroviejo M, Caumont-Sarcos A, et al. (2005) HIV-1 integrase crosslinked oligomers are active in vitro. Nucleic Acids Res 33: 977-986.
5. Li M, Mizuuchi M, Burke TR Jr, Craigie R, (2006) Retroviral DNA integration: reaction pathway and critical intermediates. EMBO J 25: 1295-1304.
6. Bao KK, Wang H, Miller JK, Erie DA, Skalka AM, et al. (2003) Functional oligomeric state of avian sarcoma virus integrase. J Biol Chem 278: 1323-1327.
7. Hare S, Gupta SS, Valkov E, Engelman A, Cherepanov P, (2010) Retroviral intasome assembly and inhibition of DNA strand transfer Nature. 464: 232-236.
8. Maertens GN, Hare S, Cherepanov P, (2010) The mechanism of retroviral integration from X-ray structures of its key intermediates. Nature 468: 326-329.
9. Gupta K, Curtis JE, Krueger S, Hwang Y, Cherepanov P, et al. (2012) Solution Conformations of Prototype Foamy Virus Integrase and Its Stable Synaptic Complex with U5 Viral DNA. Structure 20: 1918-1928.
10. Engelman A, Bushman FD, Craigie R, (1993) Identification of discrete functional domains of HIV-1 integrase and their organization within an active multimeric complex. EMBO J 12: 3269-3275.
11. van Gent DC, Vink C, Groeneger AA, Plasterk RH, (1993) Complementation between HIV integrase proteins mutated in different domains. EMBO J 12: 3261-3267.
12. Jenkins TM, Engelman A, Ghirlando R, Craigie R, (1996) A soluble active mutant of HIV-1 integrase: involvement of both the core and carboxyl-terminal domains in multimerization. J Biol Chem 271: 7712-7718.
13. Hare S, Vos AM, Clayton RF, Thuring JW, Cummings MD, et al. (2010) Molecular mechanisms of retroviral integrase inhibition and the evolution of viral resistance. Proc Natl Acad Sci U S A 107: 20057-20062.
14. Peletskaya E, Andrake M, Gustchina A, Merkel G, Alexandratos J, et al. (2011) Localization of ASV integrase-DNA contacts by site-directed crosslinking and their structural analysis. PLoS One 6: e27751.
15. Chen JC, Krucinski J, Miercke LJ, Finer-Moore JS, Tang AH, et al. (2000) Crystal structure of the HIV-1 integrase catalytic core and C-terminal domains: a model for viral DNA binding. Proc Natl Acad Sci U S A 97: 8233-8238.
16. Dyda F, Hickman AB, Jenkins TM, Engelman A, Craigie R, et al. (1994) Crystal structure of the catalytic domain of HIV-1 integrase: similarity to other polynucleotidyl transferases. Science 266: 1981-1986.
17. Wang JY, Ling H, Yang W, Craigie R, (2001) Structure of a two-domain fragment of HIV-1 integrase: implications for domain organization in the intact protein. EMBO J 20: 7333-7343.
18. Lubkowski J, Dauter Z, Yang F, Alexandratos J, Merkel G, et al. (1999) Atomic resolution structures of the core domain of avian sarcoma virus integrase and its D64N mutant. Biochemistry 38: 13512-13522.
19. Yang ZN, Mueser TC, Bushman FD, Hyde CC, (2000) Crystal structure of an active two-domain derivative of Rous sarcoma virus integrase. J Mol Biol 296: 535-548.
20. Ballandras A, Moreau K, Robert X, Confort MP, Merceron R, et al. (2011) A crystal structure of the catalytic core domain of an avian sarcoma and leukemia virus integrase suggests an alternate dimeric assembly. PLoS One 6: e23032.
21. Chen Z, Yan Y, Munshi S, Li Y, Zugay-Murphy J, et al. (2000) X-ray structure of simian immunodeficiency virus integrase containing the core and C-terminal domain (residues 50-293)-an initial glance of the viral DNA binding platform. J Mol Biol 296: 521-533.
22. Yao X, Fang S, Qiao W, Geng Y, Shen Y, (2010) Crystal structures of catalytic core domain of BIV integrase: implications for the interaction between integrase and target DNA. Protein Cell 1: 363-370.
23. Eijkelenboom AP, Lutzke RA, Boelens R, Plasterk RH, Kaptein R, et al. (1995) The DNA-binding domain of HIV-1 integrase has an SH3-like fold. Nat Struct Biol 2: 807-810.
24. Pandey KK, Bera S, Grandgenett DP, (2011) The HIV-1 Integrase Monomer Induces a Specific Interaction with LTR DNA for Concerted Integration. Biochemistry 50: 9788-9796.
25. Bushman FD, Wang B, (1994) Rous sarcoma virus integrase protein: mapping functions for catalysis and substrate binding. J Virol 68: 2215-2223.
26. Katz RA, Merkel G, Skalka AM, (1996) Targeting of retroviral integrase by fusion to a heterologous DNA binding domain: in vitro activities and incorporation of a fusion protein into viral particles. Virology 217: 178-190.
27. Hare S, Di Nunzio F, Labeja A, Wang J, Engelman A, et al. (2009) Structural basis for functional tetramerization of lentiviral integrase. PLoS Pathog 5: e1000515.
28. Alian A, Griner SL, Chiang V, Tsiang M, Jones G, et al. (2009) Catalytically-active complex of HIV-1 integrase with a viral DNA substrate binds anti-integrase drugs. Proc Natl Acad Sci U S A 106: 8192-8197.
29. Vora AC, Chiu R, McCord M, Goodarzi G, Stahl SJ, et al. (1997) 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.
30. Bojja RS, Andrake MD, Weigand S, Merkel G, Yarychkivska O, et al. (2011) 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.
31. Katzman M, Katz RA, Skalka AM, Leis J, (1989) The avian retroviral integration protein cleaves the terminal sequences of linear viral DNA at the in vivo sites of integration. J Virol 63: 5319-5327.
32. Hippenmeyer PJ, Grandgenett DP, (1984) Requirement of the avian retrovirus pp32 DNA binding protein domain for replication. Virology 137: 358-370.
33. Horton R, Mumm SR, Grandgenett DP, (1991) Phosphorylation of the avian retrovirus integration protein and proteolytic processing of its carboxyl terminus. J Virol 65: 1141-1148.
34. Chiu R, Grandgenett DP, (2003) Molecular and genetic determinants of Rous sarcoma virus integrase for concerted DNA integration. J Virol 77: 6482-6492.
35. Heuer TS, Brown PO, (1998) Photo-cross-linking studies suggest a model for the architecture of an active human immunodeficiency virus type 1 integrase-DNA complex. Biochemistry 37: 6667-6678.
36. Esposito D, Craigie R, (1998) Sequence specificity of viral end DNA binding by HIV-1 integrase reveals critical regions for protein-DNA interaction. EMBO J 17: 5832-5843.
37. Gao K, Butler SL, Bushman F, (2001) Human immunodeficiency virus type 1 integrase: arrangement of protein domains in active cDNA complexes. EMBO J 20: 3565-3576.
38. Michel F, Crucifix C, Granger F, Eiler S, Mouscadet JF, et al. (2009) Structural basis for HIV-1 DNA integration in the human genome, role of the LEDGF/P75 cofactor. EMBO J 28: 980-991.
39. Mumm SR, Horton R, Grandgenett DP, (1992) v-Src enhances phosphorylation at Ser-282 of the Rous sarcoma virus integrase. J Virol 66: 1995-1999.
40. Dar MJ, Monel B, Krishnan L, Shun MC, Di Nunzio F, et al. (2009) Biochemical and virological analysis of the 18-residue C-terminal tail of HIV-1 integrase. Retrovirology 6: 94.
41. Mohammed KD, Topper MB, Muesing MA, (2011) Sequential deletion of the integrase (Gag-Pol) carboxyl-terminus reveals distinct phenotypic classes of defective HIV-1. J Virol 85: 4654-4666.
42. Quashie PK, Mesplede T, Han YS, Oliveira M, Singhroy DN, et al. (2012) 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.
43. Otwinowski Z, Minor W, (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326.
44. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
45. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
46. Murshudov GN, vagin A, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Cryst D53: 240-255.
47. The PyMOL Molecular Graphics System (Available: http://www.pymol.org. Accessed 2013 January).
48. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA, (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98: 10037-10041.
49. McCord M, Stahl SJ, Mueser TC, Hyde CC, Vora AC, et al. (1998) Purification of recombinant Rous sarcoma virus integrase possessing physical and catalytic properties similar to virion-derived integrase. Protein Expr Purif 14: 167-177.
50. Vora A, Bera S, Grandgenett D, (2004) Structural organization of avian retrovirus integrase in assembled intasomes mediating full-site integration. J Biol Chem 279: 18670-18678.
51. Zhou H, Rainey GJ, Wong SK, Coffin JM, (2001) Substrate sequence selection by retroviral integrase. J Virol 75: 1359-1370.