Mutagenesis and homology modeling of the Tn21 integron integrase IntI1

Biochemistry

Volumn 48, Issue 8, 2009, Pages 1743-1753

  Johansson, Carolina ^a   Boukharta, Lars ^a   Eriksson, Jens ^a   Åqvist, Johan ^a   Sundström, Lars ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RESIDUES; ANTIBIOTIC RESISTANCES; BACTERIAL CHROMOSOMES; BINDING ASSAYS; CONSERVED REGIONS; DNA TRANSFERS; HOMOLOGY MODELING; HOMOLOGY MODELS; HORIZONTAL GENE TRANSFERS; HYDROGEN BONDING NETWORKS; INTEGRASE; INTEGRONS; LOCAL STABILITIES; MOBILITY SHIFT ASSAYS; MOLECULAR DYNAMICS SIMULATIONS; SPECIAL ELEMENTS; SPECIFIC CONTACTS; TARGET SITES; VIBRIO CHOLERAE;

AMINES; AMINO ACIDS; BACTERIOLOGY; DYNAMICS; ELECTROPHORESIS; GENE TRANSFER; GENES; HYDROGEN; HYDROGEN BONDS; MOLECULAR DYNAMICS; MUTAGENESIS; NUCLEIC ACIDS; ORGANIC ACIDS;

CRYSTAL STRUCTURE;

AMINO ACID; INTEGRASE; RECOMBINASE;

ARTICLE; BACTERIAL CHROMOSOME; CRYSTAL STRUCTURE; ELECTROPHORESIS; ENZYME STABILITY; ENZYME SUBSTRATE; GENE CASSETTE; HORIZONTAL GENE TRANSFER; HYDROGEN BOND; INTEGRON; MOLECULAR DYNAMICS; MUTAGENESIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN BINDING; SEQUENCE HOMOLOGY; SIMULATION; TRANSPOSON; VIBRIO CHOLERAE;

AMINO ACID SEQUENCE; ATTACHMENT SITES, MICROBIOLOGICAL; AUTORADIOGRAPHY; BIOCATALYSIS; DNA; DNA TRANSPOSABLE ELEMENTS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HYDROGEN BONDING; INTEGRASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS; MUTANT PROTEINS; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINATION, GENETIC; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY, PROTEIN; VIBRIO CHOLERAE;

BACTERIA (MICROORGANISMS); VIBRIO CHOLERAE;

EID: 64549154463     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi8020235     Document Type: Article

References (55)

1. Stokes, H. W., and Hall, R. M. (1989) A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: Integrons. Mol. Microbiol. 3, 1669-1683.
2. Hall, R. M., and Collis, C. M. (1995) Mobile gene cassettes and integrons: Capture and spread of genes by site-specific recombination. Mol. Microbiol. 15, 593-600.
3. Leverstein-van Hall, M. A., Blok, H. E. M., Donders, A. R. T., Paauw, A., Fluit, A. C., and Verhoef, J. (2003) Multidrug resistance among Enterobacteriaceae is strongly associated with the presence of integrons and is independent of species or isolate origin. J. Infect. Dis. 187, 251-259.
4. Martinez, E., and de la Cruz, F. (1990) Genetic elements involved in Tn21 site-specific integration, a novel mechanism for the dissemination of antibiotic resistance genes. EMBO J. 9, 1275-1281.
5. Sundstrom, L., Radstrom, P., Swedberg, G., and Skold, O. (1988) Site-specific recombination promotes linkage between trimethoprim and sulfonamide resistance genes. Sequence characterization of dhfrV and sulI and a recombination active locus of Tn21. Mol. Gen. Genet. 213, 191-201.
6. Mazel, D., Dychinco, B., Webb, V. A., and Davies, J. (1998) A distinctive class of integron in the Vibrio cholerae genome. Science 280, 605-608.
7. Burrus, V., and Waldor, M. K. (2004) Shaping bacterial genomes with integrative and conjugative elements. Res. Microbiol. 155, 376-386.
8. Sundstrom, L., Roy, P. H., and Skold, O. (1991) Site-specific insertion of three structural gene cassettes in transposon Tn7. J. Bacteriol. 173, 3025-3028.
9. Recchia, G. D., and Hall, R. M. (1995) Gene cassettes: A new class of mobile element. Microbiology (Reading, U.K.) 141, 3015-3027.
10. Collis, C. M., Grammaticopoulos, G., Briton, J., Stokes, H. W., and Hall, R. M. (1993) Site-specific insertion of gene cassettes into integrons. Mol. Microbiol. 9, 41-52.
11. Collis, C. M., and Hall, R. M. (1992) Gene cassettes from the insert region of integrons are excised as covalently closed circles. Mol. Microbiol. 6, 2875-2885.
12. Collis, C. M., and Hall, R. M. (1992) Site-specific deletion and rearrangement of integron insert genes catalyzed by the integron DNA integrase. J. Bacteriol. 174, 1574-1585.
13. Grindley, N. D. F., Whiteson, K. L., and Rice, P. A. (2006) Mechanisms of Site-Specific Recombination. Annu. Rev. Biochem. 75, 567-605.
14. Nash, H. A. (1996) Site-specific recombination: Integration, excision, resolution, and inversion of defined DNA segments. In Escherichia coli and Salmonella: Cellular and Molecular Biology (Neidhardt, F. C., Curtiss, R., III, Ingraham, J. L., Lin, E. C. C., Low, K. B., Magasanik, B., Reznikoff, W. S., Riley, M., Schaechter, M., and Umbarger, H. E., Eds.) 2nd ed., pp 2363-2376, ASM Press, Washington, DC.
15. Mondragon, A. (1997) Solving the cis/trans paradox in the Int family of recombinases. Nat. Struct. Biol. 4, 427-429.
16. Chaconas, G., Stewart, P., Tilly, K., Bono, J., and Rosa, P. (2001) Telomere resolution in the Lyme disease spirochete. EMBO J. 20, 3229-3237.
17. Argos, P., Landy, A., Abremski, K., Egan, J. B., Haggard-Ljungquist, E., Hoess, R. H., Kahn, M. L., Kalionis, B., Narayana, S. V., and Pierson, L. S. (1986) The integrase family of site-specific recombinases: Regional similarities and global diversity. EMBO J. 5, 433-440.
18. Nunes-Duby, S. E., Kwon, H. J., Tirumalai, R. S., Ellenberger, T., and Landy, A. (1998) Similarities and differences among 105 members of the Int family of site-specific recombinases. Nucleic Acids Res. 26, 391-406.
19. Esposito, D., and Scocca, J. J. (1997) The integrase family of tyrosine recombinases: Evolution of a conserved active site domain. Nucleic Acids Res. 25, 3605-3614.
20. Abremski, K. E., and Hoess, R. H. (1992) Evidence for a second conserved arginine residue in the integrase family of recombination proteins. Protein Eng. 5, 87-91.
21. Grainge, I., and Jayaram, M. (1999) The integrase family of recombinase: Organization and function of the active site. Mol. Microbiol. 33, 449-456.
22. Yang, W., and Mizuuchi, K. (1997) Site-specific recombination in plane view. Structure 5, 1401-1406.
23. Guo, F., Gopaul, D. N., and van Duyne, G. D. (1997) Structure of Cre recombinase complexed with DNA in a site-specific recombination synapse. Nature 389, 40-46.
24. Chen, Y., Narendra, U., Iype, L. E., Cox, M. M., and Rice, P. A. (2000) Crystal structure of a Flp recombinase-Holliday junction complex: Assembly of an active oligomer by helix swapping. Mol. Cell 6, 885-897.
25. Biswas, T., Aihara, H., Radman-Livaja, M., Filman, D., Landy, A., and Ellenberger, T. (2005) A structural basis for allosteric control of DNA recombination by lambda integrase. Nature 435, 1059-1066.
26. Redinbo, M. R., Stewart, L., Kuhn, P., Champoux, J. J., and Hol, W. G. (1998) Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279, 1504-1513.
27. Kwon, H. J., Tirumalai, R., Landy, A., and Ellenberger, T. (1997) Flexibility in DNA recombination: Structure of the lambda integrase catalytic core. Science 276, 126-131.
28. Hickman, A. B., Waninger, S., Scocca, J. J., and Dyda, F. (1997) Molecular organization in site-specific recombination: The catalytic domain of bacteriophage HP1 integrase at 2.7 Å resolution. Cell 89, 227-237.
29. Subramanya, H. S., Arciszewska, L. K., Baker, R. A., Bird, L. E., Sherratt, D. J., and Wigley, D. B. (1997) Crystal structure of the site-specific recombinase, XerD. EMBO J. 16, 5178-5187.
30. Sharma, A., Hanai, R., and Mondragon, A. (1994) Crystal structure of the amino-terminal fragment of vaccinia virus DNA topoisomerase I at 1.6 Å resolution. Structure 2, 767-777.
31. Messier, N., and Roy, P. H. (2001) Integron integrases possess a unique additional domain necessary for activity. J. Bacteriol. 183, 6699-6706.
32. MacDonald, D., Demarre, G., Bouvier, M., Mazel, D., and Gopaul, D. N. (2006) Structural basis for broad DNA-specificity in integron recombination. Nature 440, 1157-1162.
33. Johansson, C., Kamali-Moghaddam, M., and Sundstrom, L. (2004) Integron integrase binds to bulged hairpin DNA. Nucleic Acids Res. 32, 4033-4043.
34. Bouvier, M., Demarre, G., and Mazel, D. (2005) Integron cassette insertion: A recombination process involving a folded single strand substrate. EMBO J. 24, 4356-4367.
35. Rowe-Magnus, D. A., Guerout, A. M., and Mazel, D. (2002) Bacterial resistance evolution by recruitment of super-integron gene cassettes. Mol. Microbiol. 43, 1657-1669.
36. Biskri, L., Bouvier, M., Guerout, A. M., Boisnard, S., and Mazel, D. (2005) Comparative study of class 1 integron and Vibrio cholerae superintegron integrase activities. J. Bacteriol. 187, 1740-1750.
37. Notredame, C., Higgins, D. G., and Heringa, J. (2000) T-Coffee: A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217.
38. Schwede, T., Kopp, J., Guex, N., and Peitsch, M. C. (2003) SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res. 31, 3381-3385.
39. Marelius, J., Kolmodin, K., Feierberg, I., and Aqvist, J. (1998) Q: A molecular dynamics program for free energy calculations and empirical valence bond simulations in biomolecular systems. J. Mol. Graphics Modell. 16, 213-225, 261.
40. MacKerell, A. D., Jr., Bashford, D., Bellott, M., Dunbrack, R. L., Jr., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, W. E., III, Roux, B., Schlenkrich, M., Smith, J. C., Stote, R., Straub, J. M., Watanabe, M., Wiórkiewicz-Kuczera, J., Yin, D., and Karplus, M. (1998) All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins. J. Phys. Chem. B 102, 3586-3616.
41. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential function for simulating liquid water. J. Chem. Phys. 79, 926-935.
42. King, G., and Warshel, A. (1989) A surface constrained all-atom solvent model for effective simulations of polar solutions. J. Chem. Phys. 91, 3647-3661.
43. Lee, F. S., and Warshel, A. (1992) A local reaction field method for fast evaluation of long-range electrostatic interactions in molecular simulations. J. Chem. Phys. 97, 3100-3107.
44. Francia, M. V., Avila, P., de la Cruz, F., and Garcia Lobo, J. M. (1997) A hot spot in plasmid F for site-specific recombination mediated by Tn21 integron integrase. J. Bacteriol. 179, 4419-4425.
45. Stokes, H. W., O'Gorman, D. B., Recchia, G. D., Parsekhian, M., and Hall, R. M. (1997) Structure and function of 59-base element recombination sites associated with mobile gene cassettes. Mol. Microbiol. 26, 731-745.
46. Barker, A., Clark, C. A., and Manning, P. A. (1994) Identification of VCR, a repeated sequence associated with a locus encoding a hemagglutinin in Vibrio cholerae O1. J. Bacteriol. 176, 5450-5458.
47. Collis, C. M., Kim, M. J., Stokes, H. W., and Hall, R. M. (1998) Binding of the purified integron DNA integrase Intl1 to integron-and cassette-associated recombination sites. Mol. Microbiol. 29, 477-490.
48. Gravel, A., Fournier, B., and Roy, P. H. (1998) DNA complexes obtained with the integron integrase IntI1 at the attI1 site. Nucleic Acids Res. 26, 4347-4355.
49. Francia, M. V., Zabala, J. C., de la Cruz, F., and Garcia Lobo, J. M. (1999) The IntI1 integron integrase preferentially binds single-stranded DNA of the attC site. J. Bacteriol. 181, 6844-6849.
50. Nield, B. S., Holmes, A. J., Gillings, M. R., Recchia, G. D., Mabbutt, B. C., Nevalainen, K. M., and Stokes, H. W. (2001) Recovery of new integron classes from environmental DNA. FEMS Microbiol. Lett. 195, 59-65.
51. Recchia, G. D., and Sherratt, D. J. (2002) Gene acquisition in bacteria by integron-mediated site-specific recombination. In Mobile DNA II (Craig, N. L., Craigie, R., Gellert, M., and Lambowitz, A. M., Eds.) 2nd ed., pp 162-176, ASM Press, Washington, DC.
52. Gillings, M., Boucher, Y., Labbate, M., Holmes, A., Krishnan, S., Holley, M., and Stokes, H. W. (2008) The Evolution of Class 1 Integrons and the Rise of Antibiotic Resistance. J. Bacteriol. 190, 5095-5100.
53. Quiroga, C., Roy, P. H., and Centrón, D. (2008) The S.ma.I2 class C group II intron inserts at integron attC sites. Microbiology (Reading, U.K.) 154, 1341-1353.
54. Demarre, G., Frumerie, C., Gopaul, D. N., and Mazel, D. (2007) Identification of key structural determinants of the IntI1 integron integrase that influence attC × attI1 recombination efficiency. Nucleic Acids Res. 35, 6475-6489.
55. Gravel, A., Messier, N., and Roy, P. H. (1998) Point mutations in the integron integrase IntI1 that affect recombination and/or substrate recognition. J. Bacteriol. 180, 5437-5442.