Differential multimerization of Moloney murine leukemia virus integrase purified under nondenaturing conditions

Virology

Volumn 316, Issue 1, 2003, Pages 146-160

  Villanueva, Rodrigo A ^a   Jonsson, Colleen B ^b   Jones, Jennifer ^a   Georgiadis, Millie M ^c   Roth, Monica J ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b NEW MEXICO STATE UNIVERSITY   (United States)

^c INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; HEPARIN; INTEGRASE; NICKEL; NITRILOTRIACETIC ACID; RECOMBINANT ENZYME; RESIN; TETRAMER; VIRUS ENZYME;

ARTICLE; BACTERIUM; GEL FILTRATION CHROMATOGRAPHY; GENE CONSTRUCT; MOLONEY LEUKEMIA ONCOVIRUS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN PURIFICATION; PROTEIN STABILITY; SYNAPSE; WILD TYPE;

BACTERIA (MICROORGANISMS); MOLONEY MURINE LEUKEMIA VIRUS; MURINAE; MURINE LEUKEMIA VIRUS;

EID: 0242384015     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0042-6822(03)00559-2     Document Type: Article

References (74)

1. Bao K.K., Wang H., Miller J.K., Erie D.A., Skalka A.M., Wong I. Functional oligomeric state of avian sarcoma virus integrase. J. Biol. Chem. 278:2003;1323-1327.
2. Brin E., Leis J. HIV-1 integrase interaction with U3 and U5 terminal sequences in vitro defined using substrates with random sequences. J. Biol. Chem. 277:2002;18357-18364.
3. Brown H., Chen H., Engelman A. Structure-based mutagenesis of the human immunodeficiency virus type 1 DNA attachment site effects on integration and cDNA synthesis . J. Virol. 73:1999;9011-9020.
4. Brown P.O., Bowerman B., Varmus H.E., Bishop J.M. Retroviral integration structure of the initial covalent product and its precursor, and a role for the viral IN protein . Proc. Natl. Acad. Sci. USA. 86:1989;2525-2529.
5. Bujacz G., Jaskolski M., Alexandratos J., Wlodawer A., Merkel G., Katz R.A., Skalka A.M. High-resolution structure of the catalytic domain of avian sarcoma virus integrase. J. Mol. Biol. 253:1995;333-346.
6. Burke C.J., Sanyal G., Bruner M.W., Ryan J.A., LaFemina R.L., Robbins H.L., Zeft A.S., Middaugh C.R., Cordingly M.G. Structural implications of spectroscopic characterization of a putative zinc finger peptide from HIV-1 integrase. J. Biol. Chem. 267:1992;9639-9644.
7. Chen J.C.-H., Krucinski J., Miercke L.J.W., Finer-Moore J.S., Tang A.H., Leavitt A.D., Stroud R.M. Crystal structure of the HIV-1 integrase catalytic core and C-terminal domains a model for viral DNA binding . Proc. Natl. Acad. Sci. USA. 97:2000;8233-8238.
8. Chen Z., Yan Y., Munshi S., Li Y., Zugay-Murphy J., Xu B., Witmer M., Felock P., Wolfe A., Sardana V., Emini E.A., Hazuda D., Kuo L.C. 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. 296:2000;521-533.
9. Cherepanov P., Maertens G., Proost P., Devreese B., Beeumen J.V., Engelborghs Y., Clercq E.D., Debyser Z. HIV-1 integrase forms stable tetramers and associates with LEDGF/p75 protein in human cells. J. Biol. Chem. 278:2003;372-381.
10. Chiu R., Grandgenett D.P. Avian retrovirus DNA internal attachment site requirements for full-site integration in vitro. J. Virol. 74:2000;8292-8298.
11. Craigie R., Fujiwara T., Bushman F. The IN protein of Moloney murine leukemia virus processes the viral DNA ends and accomplishes their integration in vitro. Cell. 62:1990;829-837.
12. Das D., Georgiadis M.M. A directed approach to improving the solubility of Moloney murine leukemia virus reverse transcriptase. Protein Sci. 10:2001;1936-1941.
13. Davies D.R., Goryshin I.Y., Reznikoff W.S., Rayment I. Three-dimensional structure of the Tn5 synaptic complex transposition intermediate. Science. 289:2000;77-85.
14. Deprez E., Tauc P., Leh H., Mouscadet J.-F., Auclair C., Bronchon J.-C. Olligomeric states of the HIV-1 integrase as measured by time-resolbed fluorescence anisotropy. Biochemistry. 39:2000;9275-9284.
15. Donzella G.A., Jonsson C.B., Roth M.J. Coordinated disintegration reactions mediated by Moloney murine leukemia virus integrase. J. Virol. 70:1996;3909-3921.
16. Donzella G.A., Leon O., Roth M.J. Implications of a central cysteine residue and the HHCC domain of Moloney murine leukemia virus integrase protein in functional multimerization. J. Virol. 72:1998;1691-1698.
17. Dotan I., Scottoline B.P., Heuer T.S., Brown P.O. Characterization of recombinant murine leukemia virus integrase. J. Virol. 69:1995;456-468.
18. Drelich M., Wilhelm R., Mous J. Identification of amino acid residues critical for endonuclease and integration activities of HIV-1 IN protein in vitro. Virology. 188:1992;459-468.
19. Dyda F., Hickman A.B., Jenkins T.M., Engelman A., Craigie R., Davies D.R. Crystal structure of the catalytic domain of HIV-1 integrase similarity to other polynucleotidyl transferases . Science. 266:1994;1981-1986.
20. Engelman A., Bushman F.D., Craigie R. Identification of discrete functional domains of HIV-1 integrase and their organization within an active multimeric complex. EMBO J. 12:1993;3269-3275.
21. Engelman A., Craigie R. Identification of conserved amino acid residues critical for human immunodeficiency virus type 1 integrase function in vitro. J. Virol. 66:1992;6361-6369.
22. Engelman A., Mizuuchi K., Craigie R. HIV-1 DNA integration mechanism of viral DNA cleavage and DNA strand transfer . Cell. 67:1991;1211-1221.
23. Espeseth A.S., Felock P., Wolfe A., Witmer M., Grobler J., Anthony N., Egbertson M., Melamed J.Y., Young S., Hamill T., Cole J.L., Hazuda D.J. HIV-1 integrase inhibitors that compete with the target DNA substrate define a unique strand transfer conformation for integrase. Proc. Natl. Acad. Sci. USA. 97:2000;11244-11249.
24. Fujiwara T., Mizuuchi K. Retroviral DNA integration structure of an integration intermediate . Cell. 54:1988;497-504.
25. Gao K., Butler S.L., Bushman F. Human immunodeficiency virus type 1 integrase arrangement of protein domains in acitve cDNA complexes . EMBO J. 20:2001;3565-3576.
26. Goodarzi G., Pursley M., Felock P., Witmer M., Hazuda D., Brackmann K., Grandgenet D. Efficiency and fidelity of full-site integration reactions using recombinant simian immunodeficiency virus integrase. J. Virol. 73:1999;8104-8111.
27. Heuer T.S., Brown P.O. Mapping features of HIV-1 integrase near selected sites on viral and target DNA molecules in an active enzyme-DNA complex by photo-cross-linking. Biochemistry. 36:1997;10655-10665.
28. Heuer T.S., Brown P.O. Photo-cross-linking studies suggest a model for the architecture of an active human immunodeficiency virus type 1 integrase-DNA complex. Biochemistry. 37:1998;6667-6678.
29. Hindmarsh P., Ridky T., Reeves R., Andrake M., Skalka A.M., Leis J. HMG protein family members stimulate human immunodeficiency virus type 1 and avian sarcoma virus concerted DNA integration in vitro. J. Virol. 73:1999;2994-3003.
30. Hyde C.C., Bushman F.D., Mueser T.C., Yang Z.-N. Crystal structure of an active two-domain derivative of rous sarcoma virus integrase. J. Mol. Biol. 296:1999;535-538.
31. Jenkins T., Kickman A., Dyda F., Ghirlando R., Davies D., Craigie R. Catalytic domain of HIV-1 integrase identification of a soluble mutant by systematic replacement of hydrophobic residues . Proc. Natl. Acad. Sci. USA. 92:1995;6057-6061.
32. Jenkins T.M., Engelman A., Ghirlando R., Craigie R. A soluble active mutant of HIV-1 integrase. J. Biol. Chem. 271:1996;7712-7718.
33. Johnson M.S., McClure M.A., Feng D.F., Gray J., Doolittle R.F. Computer analysis of retroviral pol genes assignment of enzymatic functions to specific sequences and homologies with nonviral enzymes . Proc. Natl. Acad. Sci. USA. 83:1986;7648-7652.
34. Jones D. GenTHREADER an efficient and reliable protein fold recognition method for genomic sequences . J. Mol. Biol. 287:1999;797-815.
35. Jones K.S., Coleman J., Merkel G.W., Laue T.M., Skalka A.M. Retroviral integrase functions as a multimer and can turn over catalytically. J. Biol. Chem. 287:1992;16037-16040.
36. Jonsson C., Gallegos J., Fero P., Severson W., Su X., Schmaljohn C. Purification and characterization of the Sin Nombre virus nucleocapsid protein expressed in Escherichia coli. Protein Expr. Purif. 23:2001;134-141.
37. Jonsson C.B., Donzella G.A., Gaucan E., Smith C.M., Roth M.J. Functional domains of Moloney murine leukemia virus integrase defined by mutation and complementation analysis. J. Virol. 70:1996;4585-4597.
38. Jonsson C.B., Donzella G.A., Roth M.J. Characterization of the forward and reverse integration reactions of the Moloney murine leukemia virus integrase protein purified from Escherichia coli. J. Biol. Chem. 268:1993;1462-1469.
39. Katz R.A., Merkel G., Kulkosky J., Leis J., Skalka A.M. The avian retroviral IN protein is both necessary and sufficient for integrative recombination in vitro. Cell. 63:1990;87-95.
40. Katzman M., Katz R., Skalka A.M., Leis J. The avian retroviral integration protein cleaves the terminal sequences of linear DNA at the in vivo sites of integration. J. Virol. 63:1989;5319-5327.
41. Khan E., Mack J.P., Katz R.A., Kulkosky J., Skalka A.M. Retroviral integrase domains DNA binding and the recognition of LTR sequences . Nucleic Acids Res. 19:1991;851-860.
42. Kulkosky J., Jones K.S., Katz R.A., Mack J.P.G., Skalka A.M. Residues critical for retroviral integrative recombination in a region that is highly conserved among retroviral/retrotransposon integrases and bacterial insertion sequence transposases. Mol. Cell. Biol. 12:1992;2331-2338.
43. Leavitt A.D., Shiue L., Varmus H.E. Site-directed mutagenesis of HIV-1 Integrase demonstrates differential effects on integrase function in vitro. J. Biol. Chem. 268:1993;2113-2119.
44. Lee S.P., Xiao J., Knutson J.R., Lewis M.S., Han M.K. Zn2+ promotes the self-association of human immunodeficiency virus type-1 integrase in vitro. Biochemistry. 36:1997;173-180.
45. Li Y., Yan Y., Zugay-Murphy J., Xu B., Cole J.L., Witmer M., Felock P., Wolfe A., Hazuda D., Sardana M.K., Chen Z., Kuo L.C., Sardana V.V. Purification, solution properties and crystallization of SIV integrase containing a continuous core and C-terminal domain. Acta Crystallogr. D Biol. Crystallogr. 55:1999;1906-1910.
46. Lodi P.L., Ernst J.A., Kuszewski J., Hickman A.B., Engelman A., Craigie R., Clore G.M., Grononborn A.M. Solution structure of the DNA binding domain of HIV-1 integrase. Biochemistry. 34:1995;9826-9833.
47. McCord M., Stahl S., Mueser T., Hyde C.C., Vora A., Grandgenett D. Purification of recombinant Rous sarcoma virus integrase possessing physical and catalytic properties similar to virion-derived integrase. Protein Expr. Purif. 14:1998;167-177.
48. McEuen A.R., Edward B., Koepke D.A., Ball A.E., Jennings B.A., Wolstenholme A.J., Danson M.J., Hough D.W. Zinc binding by retroviral integrase. Biochem. Biophys. Res. Commun. 189:1992;813-818.
49. Mumm S.R., Grandgenett D.P. Defining nucleic acid-binding properties of avian retrovirus integrase by deletion analysis. J. Virol. 65:1991;1160-1167.
50. Murphy J.E., Goff S.P. A mutation at one end of Moloney murine leukemia virus DNA blocks cleavage of both ends by the viral integrase in vivo. J. Virol. 66:1992;5092-5095.
51. Piefer A., Jonsson C.B. A comparative study of the human T-cell leukemia virus type 2 integrase expressed in and purified from Escherichia coli and Pichia pastoris. Protein Exp. Purif. 25:2002;291-299.
52. Roth M.J., Schwartzberg P., Tanese N., Goff S.P. Analysis of mutations in the integration function of Moloney murine leukemia virus effects on DNA binding and cutting . J. Virol. 64:1990;4709-4717.
53. Roth M.J., Schwartzberg P.L., Goff S.P. Structure of the termini of DNA intermediates in the integration of retroviral DNA dependence of IN function and terminal DNA sequence . Cell. 58:1989;47-54.
54. Roth M.J., Tanese N., Goff S.P. Gene product of Moloney murine leukemia virus required for proviral integration is a DNA-binding protein. J. Mol. Biol. 203:1988;131-139.
55. Sherman P.A., Fyfe J.A. Human immunodeficiency virus integration protein expressed in Escherichia coli possesses selective DNA cleavage activity. Proc. Natl. Acad. Sci. USA. 87:1990;5119-5123.
56. Shibagaki Y., Holmes M.L., Appa R.S., Chow S.A. Characterization of Feline immunodeficiency virus integrase and analysis of functional domains. Virology. 230:1997;1-10.
57. Sinha S., Pursley M.H., Grandgenett D.P. Efficient concerted integration by recombinant human immunodeficiency virus type 1 integrase without cellular or viral cofactors. J. Virol. 76:2002;3105-3113.
58. Tanese N., Roth M.J., Goff S.P. Analysis of retroviral pol gene products with antisera raised against fusion proteins produced in Escherichia coli. J. Virol. 59:1986;328-340.
59. VanDenEnt F.M.I., Vos A., Plasterk R.H.A. Dissecting the role of the N-terminal domain of human immunodeficiency virus integrase by trans-complementation analysis. J. Virol. 73:1999;3176-3183.
60. vanGent D.C., Vink C., Groeneger A.A.M.O., Plasterk R.H.A. Complementation between HIV integrase proteins mutated in different domains. EMBO J. 12:1993;3261-3267.
61. Vercammen J., Maertens G., Gerard M., Clercq E.D., Debyser Z., Engelborghs Y. DNA-induced polymerization of HIV-1 integrase analyzed with fluorescence fluctuation spectroscopy. J. Biol. Chem. 277:2002;38052-38405.
62. Vincent K.A., Ellison V., Chow S.A., Brown P.O. Characterization of human immunodeficiency virus type 1 integrase expressed in Escherichia coli and analysis of variants with amino-terminal mutations. J. Virol. 67:1993;425-437.
63. Vink C., Groeneger A.A.M.O., Plasterk R.H.A. Identification of the catalytic and DNA-binding region of the human immunodeficiency virus type 1 integrase protein. Nucleic. Acids. Res. 21:1993;1419-1425.
64. Vink C., Lutzke R.A., Plasterk R.H.A. Formation of a stable complex between the human immunodeficiency virus integrase protein and viral DNA ends. Nucleic Acids Res. 22:1994;4103-4110.
65. Vink C., VanGent D.C., Elgersma Y., Plasterk R.H.A. Human immunodeficiency virus integrase protein requires a subterminal position of its viral DNA recognition sequence for efficient cleavage. J. Virol. 65:1991;4636-4644.
66. 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. 20:2001;7333-7343.
67. Wei S.-Q., Mizuuchi K., Craigie R. Footprint on the viral DNA ends in Moloney murine leukemia virus preintegration complexes reflect a specific association with integrase. Proc. Natl. Acad. Sci. USA. 95:1998;10535-10540.
68. Woerner A.M., Marcus-Sekura C.J. Characterization of a DNA binding domain in the C-terminus of HIV-1 integrase by deletion mutagenesis. Nucleic Acids Res. 21:1993;3507-3511.
69. Wolfe A.L., Felock P.J., Hastings J.C., Blau C.U., Hazuda D.J. The role of manganese in promoting multimerization and assembly of human immunodeficiency virus type 1 integrase as a catalytically active complex on immobilized long terminal repeat substrates. J. Virol. 70:1996;1424-1432.
70. Yang F., Leon O., Greenfield N.J., Roth M.J. Functional interactions of the HHCC domain of Moloney murine leukemia virus integrase revealed by non-overlapping complementation and zinc dependent dimerization. J. Virol. 73:1999;1809-1817.
71. Yang F., Roth M.J. Assembly and catalysis of concerted two-end integration events by Moloney murine leukemia virus integrase. J. Virol. 75:2001;9561-9570.
72. Yang Z.-N., Mueser T., Bushman F., Hyde C.C. Crystal structure of an active two-domain derivative of Rous sarcoma virus integrase. J. Mol. Biol. 296:1999;535-548.
73. Yang Z.N., Mueser T.C., Hyde F.D.B.C.C. Crystal structure of an active two-domain derivative of Rous sarcoma virus integrase. J. Mol. Biol. 296:2000;535-548.
74. Zheng R., Jenkins T.M., Craigie R. Zinc folds the N-terminal domain of HIV-1 integrase, promotes multimerization, and enhances catalytic activity . Proc. Natl. Acad. Sci. USA. 93:1996;13659-13664.