Site-directed mutagenesis of the catalytic residues of bovine pancreatic deoxyribonuclease I

Journal of Molecular Biology

Volumn 264, Issue 5, 1996, Pages 1154-1163

  Jones, Stephen J ^a   Worrall, Andrew F ^b   Connolly, Bernard A ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Acid base catalysis; DNase I; Electrophilic catalysis; Phosphodiester bond hydrolysis; Site directed mutagenesis

Indexed keywords

DEOXYRIBONUCLEASE I; DNA; MAGNESIUM ION; MUTANT PROTEIN; PANCREAS ENZYME;

AMINO ACID SEQUENCE; ARTICLE; CATTLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION;

EID: 17044447168     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0703     Document Type: Article

References (63)

1. Ariyoshi, M., Vassylyev, D. G., Iwasaki, H., Nakamura, H., Shinagawa, H. & Morikawa, K. (1994). Atomic structure of the RuvC resolvase: a Holliday junction-specific endonuclease from E. coli. Cell, 78, 1063-1072.
2. 1 2′-GMP complex at 1.9 Å resolution. J. Biol. Chem. 263, 15358-15368.
3. 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.
4. 15 NMR spectroscopy of hydrogen bonding interactions in the active site of serine proteases: evidence for a moving histidine mechanism. Biochemistry, 25, 7751-7759.
5. Beese, L. S. & Steitz, T. A. (1991). Structural basis for the 3′-5′ exonuclease activity of Escherichia coli DNA polymerase I: a two metal ion mechanism. EMBO J. 10, 25-33.
6. Borah, B., Chen, C. W., Egan, W., Miller, A., Wlodawer, A. & Cohen, J. S. (1985). Nuclear magnetic resonance and neutron diffraction studies of the complex of ribonuclease A with uridine vanadate, a transiton state analogue. Biochemistry, 24, 2058-2067.
7. Brosius, J. & Holy, A. (1984). Regulation of ribosomal RNA promoters with a synthetic lac operator. Proc. Natl Acad. Sci. USA, 81, 6929-8169.
8. Campbell, R. L. & Petsko, G. A. (1987). Ribonuclease structure and catalysis: crystal structure of sulfate free native ribonuclease A at 1.5 Å resolution. Biochemistry, 26, 8579-8584.
9. Cheng, X., Baiendiran, K., Schildkraut, I. & Anderson, I. (1994). Structure of PvuII endonuclease with cognate DNA. EMBO J. 13, 3927-3935.
10. Chin, J., Banaszczyk, F., Jubian, V. & Zou, X. (1989). Co(III) complex promoted hydrolysis of phosphate diesters: comparison in reactivity of rigid cis-diaquotetraazacobalt(III) complexes. J. Am. Chem. Soc. 111, 186-190.
11. Cotton, F. A., Hazen, E. E. & Legg, M. J. (1979). Staphylococcal nuclease: proposed mechanism of action based on structure of enzyme-thymidine-3′,5′-bisphosphate-calcium ion complex at 1.5 Å resolution. Proc. Natl Acad. Sci. USA, 76, 2551-2555.
12. Davies, J. F., Hostomska, Z., Hostomsky, Z., Jordan, S. R. & Matthews, D. A. (1991). Crystal structure of the ribonuclease H domain of HIV-1 reverse transcriptase. Science, 252, 82-95.
13. del Rosario, E. J. & Hammes, G. G. (1969). Kinetic and equilibrium studies of the ribonuclease catalysed hydrolysis of uridine 2′-3′ cyclic phosphate. Biochemistry, 8, 1884-1889.
14. Doherty, A. J., Worrall, A. F. & Connolly, B. A. (1991). Mutagenesis of the DNA binding residues in bovine pancreatic DNase I: an investigation into the mechanism of sequence descrimination by a sequence selective nuclease. Nucl. Acids Res. 19, 6129-6132.
15. Doherty, A. J., Connolly, B. A. & Worrall, A. F. (1993). Overproduction of the toxic protein, bovine pancreatic DNase I, in Escherichia coli using a tightly controlled T7-promoter based system. Gene, 136, 337-340.
16. Doherty, A. J., Worrall, A. F. & Connolly, B. A. (1995). The roles of arginine 41 and tyrosine 76 in the coupling of DNA recognition to phosphodiester bond cleavage by DNase I: a study using site-directed mutagenesis. J. Mol. Biol. 251, 366-377.
17. Drew, H. R. & Travers, A. A. (1984). DNA structural variations in the E.coli Tyr T promoter. Cell, 37, 491-502.
18. Dyda, F., Hickman, A. B., Jenkins, T. M., Engelman, A., Craigie, R. & Davies, D. R. (1994). Crystal structure of the catalytic domain of HIV-1 integrase: similarity to other polynucleotidyl transferases. Science, 266, 1981-1986.
19. Fersht, A. (1985). Enzyme Structure and Mechanism, 2nd edit., W. H. Freeman and Co., New York.
20. Findlay, D., Herries, D. G., Mathias, A. D., Rabin, B. R. & Ross, C. A. (1961). The active site and mechanism of action of bovine pancreatic ribonuclease. Nature, 190, 781-784.
21. Gerlt, J. A. (1993). Mechanistic principles of enzyme-catalysed cleavage of phosphodiester bonds. In Nucleases, (Linn, S. M., Lloyd, R. S. & Roberts, R. J., eds), 2nd edit., pp. 1-34, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
22. Hartsuck, J. A. & Lipscomb, W. N. (1971). Carboxypeptidase A. In The Enzymes (Boyer, P. D., ed.), 3rd edit., vol. 3, pp. 1-56, Academic Press, New York.
23. 1-2′-guanylic acid complex: an X-ray structure. Nature, 299, 27-31.
24. Knowles, J. R. (1991). Enzyme catalysis: not different, just better. Nature, 350, 121-124.
25. 2+ binding to the active-site of EcoRV endonuclease-a crystallographic study of complexes with substrates and products at 2 Ångstrom resolution. Biochemistry, 34, 683-696.
26. Kunitz, M. (1950). Crystalline deoxyribonuclease I. Isolation and general properties: spectrophotometric method for the measurement of deoxyribonuclease activity. J. Gen. Physiol. 33, 363-377.
27. Kunkel, T. A. (1985). Rapid and efficient site-directed mutagenesis without phenotypic selection. Proc. Natl Acad. Sci. USA, 82, 488-492.
28. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
29. Lahm, A. & Suck, D. (1991). DNase I-induced DNA conformation. 2 Å structure of a DNase I octamer complex. J. Mol. Biol. 222, 645-667.
30. Laskowski, M. (1971). Deoxyribonuclease I. In The Enzymes (Boyer, P. D., ed.), 3rd edit. vol. 4, pp. 289-311, Academic Press, New York.
31. Lewendon, A., Murray, I. A. & Shaw, W. V. (1994). Replacement of catalytic histidine-195 of chloramphenicol acetyltransferase: evidence for a general base role for glutamate. Biochemistry, 33, 1944-1950.
32. Liao, T. H. (1975). Deoxythymidine 3′,5′-di-p-nitrophenyl phosphate as a synthetic substrate for bovine pancreatic deoxyribonuclease. J. Biol. Chem. 250, 3721-3724.
33. Liao, T.-H., Salnikow, J., Moore, S. & Stein, W. H. (1973). Bovine pancreatic deoxyribonuclease A. Isolation of cyanogen bromide peptides; complete covalent structure of the polypeptide chains. J. Biol. Chem. 248, 1489-1495.
34. Liao, T.-H., Ho, H.-C. & Abe, A. (1991). Chemical modification of bovine pancreatic DNase with phenylglyoxal. The involement of Arg-9 and Arg-41 in substrate binding. Biochim. Biophys. Acta, 1079, 335-342.
35. Lodi, P. J. & Knowles, J. R. (1991). Neutral imidazole is the electrophile in the reaction catalysed by triose phosphate isomerase: structural origins and catalytic implications. Biochemistry, 30, 6948-6986.
36. 2+, and the inhibitor pdTp, refined to 1.65 Å. Proteins: Struct. Funct. Genet. 5, 183-201.
37. Markley, J. L. (1975). Correlation proton magnetic resonance studies at 250 MHz of bovine pancreatic ribonuclease I. Reinvestigation of histidine peak assignments. Biochemistry, 14, 3546-3554.
38. 18O]phosphates and the stereochemical course of the reaction catalysed by deoxyribonuclease I. Biochemistry, 23, 4844-4852.
39. Mol, C. D., Kuo, C-F., Thayer, M. M., Cunningham, R. P. & Tainer, J. A. (1995). Structure and function of the multifunctional DNA-repair enzyme exonuclease III. Nature, 374, 381-386.
40. Moore, S. (1981). In The Enzymes (Boyer, P. D., ed.), 3rd edit. vol. 14, pp. 281-296, Academic Press, New York.
41. Newman, M., Strzelecka, T., Dorner, L. F., Schildkraut, I. & Aggarwal, A. K. (1995). Structure of Bam HI endonuclease bound to DNA-partial folding and unfolding on DNA binding. Science, 269, 656-663.
42. O'Connor, C. D. & Timmis, K. N. (1987). Highly repressible expression system for cloning genes that specify potentially toxic proteins. J. Bacteriol. 169, 4457-4462.
43. 1: kinetic studies using GpA, GpC, GpG and GpU as substrates. Biochemistry, 17, 4124-4130.
44. Paudel, H. K. & Liao, T. H. (1986). Comparison of the three primary structures of deoxyribonuclease isolated from bovine, ovine and porcine pancreas. J. Biol. Chem. 261, 16012-16017.
45. a values of two histidine residues in human haemoglobin, the Bohr effects and the dipole moment of α-helices. J. Mol. Biol. 192, 605-632.
46. Polzar, B. & Mannherz, H. G. (1990). Nucleotide sequence of a full length cDNA clone encoding the deoxyribonuclease I from the rat parotid gland. Nucl. Acids Res. 18, 7151.
47. Pourmotabbed, T., Dell'Aqua, M., Gerlt, J. A., Stanczyk, S. M. & Bolton, P. H. (1990). Kinetic and conformational effects of lysine substitutions for arginines 35 and 87 in the active site of staphylococcal nuclease. Biochemistry, 29, 3677-3683.
48. 2+ in the activity of bovine pancreatic deoxyribonuclease. J. Biol. Chem. 250, 1981-1986.
49. Price, P. A., Moore, S. & Stein, W. H. (1969). Alkylation of a histidine residue at the active site of bovine pancreatic deoxyribonuclease. J. Biol. Chem. 244, 924-928.
50. Sayers, J. R. & Eckstein, F. (1991). A single-strand specific endonuclease activity co-purifies with overexpressed T5 D15 exonuclease. Nucl. Acids Res. 19, 4127-4132.
51. Shak, S., Capon, D. J., Hellmiss, R., Marsters, S. A. & Baker, C. L. (1990). Recombinant human DNase I reduces the viscosity of cystic fibrosis sputum. Proc. Natl Acad. Sci. USA, 87, 9188-9192.
52. Steitz, T. A. (1993). DNA- and RNA dependent polymerases. Curr. Opin. Struct. Biol. 3, 31-38.
53. Steitz, T. A. & Steitz, J. A. (1993). A general two-metal-ion mechanism for catalytic RNA. Proc. Natl Acad. Sci. USA, 90, 6498-6502.
54. 1 acts as a base catalyst when the true catalytic base, glutamic acid-58 is replaced by alanine. Biochemistry, 29, 9064-9072.
55. Suck, D. & Oefner, C. (1986). Structure of DNase I at 2 Å resolution suggests a mechanism for binding to and cutting DNA. Nature, 321, 620-625.
56. Suck, D., Oefner, C. & Kabsch, W. (1984). Three-dimensional structure of bovine pancreactic DNase I at 2.5 Å resolution. EMBO J. 3, 2423-2430.
57. Suck, D., Lahm, A. & Oefner, C. (1988). Structure refined to 2 Å of a nicked DNA oligonucleotide complex with DNase I. Nature, 332, 465-468.
58. Tanford, C. (1962). The interpretation of hydrogen ion titration curves of proteins. Advan. Protein Chem. 17, 69-165.
59. Vipond, I. B., Baldwin, G. S. & Halford, S. E. (1995). Divalent metal ions at the active sites of the EcoRV and EcoRI restriction endonucleases. Biochemistry, 34, 697-704.
60. Weston, S. & Suck, D. (1993). X-ray structure of two single-residue mutants of DNase I: H134Q and Y76A. Protein Eng. 6, 349-357.
61. Weston, S., Lahm, A. & Suck, D. (1992). X-ray structure of the DNase I-d(GGTATACC). complex at 2.3 Å resolution. J. Mol. Biol. 226, 1237-1256.
62. Worrall, A. & Connolly, B. A. (1990). The chemical synthesis of a gene coding for bovine pancreatic DNase I and its cloning and expression in E coli. J. Biol. Chem. 265, 21889-21895.
63. Yang, W. & Steitz, T. A. (1995). Recombining the structures of HIV integrase, RuvC and RNase H. Structure, 3, 131-134