Asp34 of PvuII endonuclease is directly involved in DNA minor groove recognition and indirectly involved in catalysis

Journal of Molecular Biology

Volumn 284, Issue 5, 1998, Pages 1491-1504

  Horton, John R ^a   Nastri, Horacio G ^b   Riggs, Paul D ^b   Cheng, Xiaodong ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW ENGLAND BIOLABS   (United States)

Author keywords

Asymmetric active sites; Catalytic water structure; DNA minor groove protein interaction; Restriction enzyme

Indexed keywords

ASPARTIC ACID; DOUBLE STRANDED DNA; ENDONUCLEASE; GLYCINE; GUANINE; MAGNESIUM ION; OLIGODEOXYNUCLEOTIDE;

ARTICLE; CATALYSIS; CODON; CONTROLLED STUDY; DNA SEQUENCE; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME STRUCTURE; ENZYME SUBUNIT; PRIORITY JOURNAL; PROTEIN DNA INTERACTION;

EID: 0032545161     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2269     Document Type: Article

References (61)

1. Aggarwal, A. K. (1995). Structure and function of restriction endonucleases. Curr. Opin. Struct. Biol. 5, 11-19.
2. Alves, J., Selent, U. & Wolfes, H. (1995). Accuracy of the EcoRV restriction endonuclease: binding and cleavage studies with oligodeoxynucleotide substrates containing degenerate recognition sequences. Biochemistry, 34, 11191-11197.
3. Anderson, J. E. (1993). Restriction endonucleases and modification methylases. Curr. Opin. Struct. Biol. 3, 24-30.
4. Athanasiadis, A., Gregoriu, M., Thanos, D., Kokkinidis, M. & Papamatheakis, J. (1990). Complete nucleotide sequence of the PvuII restriction enzyme gene from Proteus vulgaris. Nucl. Acids Res. 18, 6434.
5. Athanasiadis, A., Vlassi, M., Kotsifaki, D., Tucker, P. A., Wilson, K. S. & Kokkinidis, M. (1994). Crystal structure of PvuII endonuclease reveals extensive structural homologies to EcoRV. Nature Struct. Biol. 1, 469-475.
6. Balendiran, K., Bonventre, J., Knott, R., Jack, W., Benner, J., Schildkraut, I. & Anderson, J. E. (1994). Expression, purification, and crystallization of restriction endonuclease PvuII with DNA containing its recognition site. Proteins: Struct. Funct. Genet. 19, 77-79.
7. Ban, C. & Yang, W. (1998). Structural basis for MutH activation in E. coli mismatch repair and relationship of MutH to restriction endonucleases. EMBO J. 17, 1526-1534.
8. Blumenthal, R. M., Gregory, S. A. & Cooperider, J. S. (1985). Cloning of a restriction-modification system from Proteus vulgaris and its use in analyzing a methylase-sensitive phenotype in Escherichia coli. J. Bacteriol. 164, 501-509.
9. Borden, K. L. (1993). The activating transcription factor region within the E2A promoter exists in a novel conformation. Biochemistry, 32, 6506-6514.
10. Borden, K. L. (1994). Two mutant binding sites of the activating transcription factor region within the E2A promoter of adenovirus exist in a novel conformation. Biochim. Biophys. Acta, 1219, 505-514.
11. Brennan, R. G. & Matthews, B. W. (1989a). The helix-turn-helix DNA binding motif. J. Biol. Chem. 264, 1903-1906.
12. Brennan, R. G. & Matthews, B. W. (1989b). Structural basis of DNA-protein recognition. Trends Biochem. Sci. 14, 286-290.
13. Brooks, B., Bruccoleri, R., Olafson, B., States, D., Swaminathan, S. & Karplus, M. (1983). CHARMM: a program for macromolecular energy, minimization, and molecular dynamics calculations. J. Comp. Chem. 4, 187-217.
14. Brünger, A. T. (1992). XPLOR, A System for X-ray Crystallography and NMR, Version 3.1, Yale University Press, New Haven, CT.
15. Brünger, A. T. (1997). Free R Value: cross-validation in crystallography. Methods Enzymol. 277, 366-395.
16. Butkus, V., Klimasauskas, S., Petrauskiene, L., Maneliene, Z., Lebionka, A. & Janulaitis, A. (1987). Interaction of AluI, Cfr6I and PvuII restriction-modification enzymes with substrates containing either N4-methylcytosine or 5-methylcytosine. Biochim. Biophys. Acta, 909, 201-207.
17. Carson, M. (1997). Ribbons. Methods Enzymol. 277, 493-504.
18. Cheng, X., Balendiran, K., Schildkraut, I. & Anderson, J. E. (1994). Structure of PvuII endonuclease with cognate DNA. EMBO J. 13, 3927-3935.
19. Dodson, E. J., Winn, M. & Ralph, A. (1997). Collaborative Computational Project. Number 4: providing programs for protein crystallography. Methods Enzymol. 277, 620-633.
20. Engh, R. A. & Huber, R. (1991). Accurate bond and angle parameters for X-ray protein-structure refinement. Acta Crystallog. sect. A, 47, 392-400.
21. Gingeras, T. R., Greenough, L., Schildkraut, I. & Roberts, R. J. (1981). Two new restriction endonucleases from Proteus vulgaris. Nucl. Acids Res. 9, 4525-4536.
22. Grabowski, G., Maass, G. & Alves, J. (1996). Asp-59 is not important for the catalytic activity of the restriction endonuclease EcoRI. FEBS Letters, 381, 106-110.
23. Horton, J. R., Bonventre, J. & Cheng, X. (1998). How is modification of the DNA substrate recognized by the PvuII restriction endonuclease? Biol. Chem. 379, 451-458.
24. Humphrey, W., Dalke, A. & Schulten, K. (1996). VMD - visual molecular dynamics. J. Mol. Graph. 14, 33-38.
25. Jeltsch, A., Alves, J., Wolfes, H., Maass, G. & Pingoud, A. (1993). Substrate-assisted catalysis in the cleavage of DNA by the EcoRI and EcoRV restriction enzymes. Proc. Natl Acad. Sci. USA, 90, 8499-8503.
26. Jen-Jacobson, L. (1997). Protein-DNA recognition complexes: conservation of structure and binding energy in the transition state. Biopolymers, 44, 153-180.
27. Jen-Jacobson, L., Engler, L. E., Lesser, D. R., Kurpiewski, M. R., Yee, C. & McVerry, B. (1996). Structural adaptations in the interaction of EcoRI endonuclease with methylated GAATTC sites. EMBO J. 15, 2870-2882.
28. Jones, T. A., Zou, J. Y., Cowan, S. W. & Kjeldgaard, M. (1991). Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A, 47, 110-119.
29. Kabsch, W. (1976). A solution for the best rotation to relate two sets of vectors. Acta. Crystallog. sect. A, 32, 922-923.
30. Kielkopf, C. L., White, S., Szewczyk, J. W., Turner, J. M., Baird, E. E., Dervan, P. B., & Rees, D. C. (1998). A structural basis for recognition of A·T and T·A base pairs in the minor groove of B-DNA. Science, 282, 111-115.
31. Kim, Y. C., Grable, J. C., Love, R., Greene, P. J. & Rosenberg, J. M. (1990). Refinement of EcoRI endonuclease crystal structure: a revised protein chain tracing. Science, 249, 1307-1309.
32. 2+ binding to the active site of EcoRV endonuclease: a crystallographic study of complexes with substrate and product DNA at 2 Å resolution. Biochemistry, 34, 683-696.
33. Kovall, R. & Matthews, B. W. (1997). Toroidal structure of lambda-exonuclease. Science, 277, 1824-1827.
34. Lesser, D. R., Kurpiewski, M. R. & Jen-Jacobson, L. (1990). The energetic basis of specificity in the EcoRI endonuclease-DNA interaction. Science, 250, 776-786.
35. McPherson, A., Jr. (1976). The growth and preliminary investigation of proteins and nucleic acid crystals for X-ray diffraction analysis. Methods Biochem. Anal. 23, 249-345.
36. Matthews, B. W. (1988). Protein-DNA interaction. No code for recognition. Nature, 335, 294-295.
37. Nastri, H. G., Evans, P. D., Walker, I. H. & Riggs, P. D. (1997). Catalytic and DNA binding properties of PvuII restriction endonuclease mutants. J. Biol. Chem. 272, 25761-25767.
38. + binding sites. J. Mol. Biol. 256, 228-234.
39. Newman, M., Strzelecka, T., Dorner, L. F., Schildkraut, I. & Aggarwal, A. K. (1994a). Structure of restriction endonuclease BamHI and its relationship to EcoRI. Nature, 368, 660-664.
40. Newman, M., Strzelecka, T., Dorner, L. F., Schildkraut, I. & Aggarwal, A. K. (1994b). Structure of restriction endonuclease BamHI phased at 1.95 A resolution by MAD analysis. Structure, 2, 439-452.
41. Newman, M., Strzelecka, T., Dorner, L. F., Schildkraut, I. & Aggarwal, A. K. (1995). Structure of BamHI endonuclease bound to DNA: partial folding and unfolding on DNA binding. Science, 269, 656-663.
42. Otwinowski, Z. & Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 277, 307-326.
43. Otwinowski, Z., Schevitz, R. W., Zhang, R. G., Lawson, C. L., Joachimiak, A., Marmorstein, R. Q., Luisi, B. F. & Sigler, P. B. (1988). Crystal structure of trp repressor/operator complex at atomic resolution. Nature, 335, 321-329.
44. Parkinson, G., Vojttechovsky, J., Clowney, L., Brünger, A. T. & Berman, H. M. (1996). New parameters for the refinement of nucleic acid containing strructures. Acta Crystallog. sect. D, 52, 57-64.
45. Pauling, L. (1960). The Nature of the Chemical Bond, Cornell University Press, Ithaca, NY.
46. Pingoud, A. & Jeltsch, A. (1997). Recognition and cleavage of DNA by type-II restriction endonucleases. Eur. J. Biochem. 246, 1-22.
47. Rice, M. R., Calvin-Koons, M. D. & Blumenthal, R. M. (1995). The PvuII (CAGCTG) endonuclease binds to and cleaves CAG5mCTG sites. FASEB J. 9, A1400.
48. Roberts, R. J. & Halford, S. E. (1993). Type II restriction enzymes. In Nucleases (Linn, S. M., Lloyd, R. S. & Roberts, R. J., eds), pp. 35-88, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
49. Robinson, C. R. & Sligar, S. G. (1998). Changes in solvation during DNA binding and cleavage are critical to altered specificity of the EcoRI endonuclease. Proc. Natl Acad. Sci. USA, 95, 2186-2191.
50. Rosenberg, J. M. (1991). Structure and function of restriction endonucleases. Curr. Opin. Struct. Biol. 1, 104-113.
51. Saenger, W. (1983). Principles of Nucleic Acid Structure, Springer-Verlag Inc., NY.
52. Schwabe, J. W. (1997). The role of water in protein-DNA interactions. Curr. Opin. Struct. Biol. 7, 126-134.
53. Seeman, N. C., Rosenberg, J. M. & Rich, A. (1976). Sequence-specific recognition of double helical nucleic acids by proteins. Proc. Natl Acad. Sci. USA, 73, 804-808.
54. Stahl, F., Wende, W., Jeltsch, A. & Pingoud, A. (1996). Introduction of asymmetry in the naturally symmetric restriction endonuclease EcoRV to investigate intersubunit communication in the homodimeric protein. Proc. Natl Acad. Sci. USA, 93, 6175-6180.
55. Stahl, F., Wende, W., Wenz, C., Jeltsch, A. & Pingoud, A. (1998). Intra- vs intersubunit communication in the homodimeric restriction enzyme EcoRV: Thr 37 and Lys 38 involved in indirect readout are only important for the catalytic activity of their own subunit. Biochemistry, 37, 5682-5688.
56. Tao, T. & Blumenthal, R. M. (1992). Sequence and characterization of pvuIIR, the PvuII endonuclease gene, and of pvuIIC, its regulatory gene. J. Bacteriol. 174, 3395-3398.
57. Thielking, V., Alves, J., Fliess, A., Maass, G. & Pingoud, A. (1990). Accuracy of the EcoRI restriction endonuclease: binding and cleavage studies with oligodeoxynucleotide substrates containing degenerate recognition sequences. Biochemistry, 29, 4682-4691.
58. Viadiu, H. & Aggarwal, A. K. (1998). The role of metals in catalysis by the restriction endonuclease BamHI. Nature Struct. Biol. 5, 910-916.
59. Wilson, G. G. & Murray, N. E. (1991). Restriction and modification systems. Annu. Rev. Genet. 25, 585-627.
60. Winkler, F. K. (1992). Structure and function of restriction endonucleases. Curr. Opin. Struct. Biol. 2, 93-99.
61. Winkler, F. K., Banner, D. W., Oefner, C., Tsernoglou, D., Brown, R. S., Heathman, S. P., Bryan, R. K., Martin, P. D., Petratos, K. & Wilson, K. S. (1993). The crystal structure of EcoRV endonuclease and of its complexes with cognate and non-cognate DNA fragments. EMBO J. 12, 1781-1795.