The DNA/RNA non-specific Serratia nuclease prefers double-stranded A-form nucleic acids as substrates

Journal of Molecular Biology

Volumn 288, Issue 3, 1999, Pages 377-390

  Meiss, Gregor ^a   Gast, Frank Ulrich ^a   Pingoud, Alfred M ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Endonuclease; Nucleic acid structure; Sequence preferences; Steady state kinetics

Indexed keywords

DOUBLE STRANDED DNA; DOUBLE STRANDED RNA; ENDONUCLEASE; PURINE; PYRIMIDINE;

ARTICLE; CIRCULAR DICHROISM; DNA CONFORMATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SUBSTRATE COMPLEX; NONHUMAN; PRIORITY JOURNAL; RNA CONFORMATION; SERRATIA MARCESCENS;

SERRATIA MARCESCENS;

EID: 0033532211     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.2694     Document Type: Article

References (64)

1. Ball T. K., Saurugger P. N., Benedik M. J. The extracellular nuclease gene of Serratia marcescens and its secretion from Escherichia coli. Gene. 57:1987;183-192.
2. Ball T. K., Sih Y., Benedik M. J. Disulfide bonds are required for Serratia marcescens nuclease activity. Nucl. Acids Res. 20:1992;4971-4974.
3. Beliaeva M. I., Kapranova M. N., Vitol M. I., Golubenko I. A., Leshchinskaia I. B. Nucleic acids utilized as the main source of bacterial nutrition. Mikrobiologiia. 45:1976;420-424.
4. Benedik M. J., Strych U. Serratia marcescens and its extracellular nuclease. FEMS Microbiol. Letters. 165:1998;1-13.
5. Berman H. M. Crystal studies of B -DNA: the answers and questions. Biopolymers. 44:1997;23-44.
6. Brukner I., Sanchez R., Suck D., Pongor S. Sequence-dependent bending propensity of DNA as revealed by DNaseI: parameters for trinucleotides. EMBO J. 14:1995;1812-1818.
7. Butkus V., Klimasauskas S., Petrauskiene L., Maneliene Z., Janulaitis A., Minchenkova L. E., Schyolkina A. K. Synthesis and physical characterization of DNA fragments containing N4-methylcytosine and 5-methylcytosine. Nucl. Acids Res. 15:1987;8467-8478.
8. Camerman N., Fawcett J. K., Camerman A. Molecular structure of a deoxyribose-dinucleotide, sodium thymidylyl-5′-3′-thymidylate-5′ hydrate (pTpT) and a possible structural model for polythymidylate. J. Mol. Biol. 107:1976;601-621.
9. Cheatham T. E., Kollman P. A. Molecular dynamics simulation highlight the structural differences among DNA:DNA, RNA:RNA and DNA:RNA hybrid duplexes. J. Am. Chem. Soc. 119:1997;4805-4825.
10. Cheng D. M., Dhingra M. M., Sarma R. H. Spatial configuration of deoxyribonucleoside diphosphate in aqueous solution. Nucl. Acids Res. 5:1978;4399-4416.
11. 2. Nucl. Acids Res. 25:1997;2627-2643.
12. nsequences by endonuclease G. J. Biol. Chem. 265:1989;3301-3310.
13. Dake E., Hofmann T. J., McIntire S., Hudson A., Zassenhaus H. P. Purification and properties of the major nuclease from mitochondria of Saccharomyces cerevisiae. J. Biol. Chem. 263:1988;7691-7702.
14. Doherty A. J., Worrall A. F., Connolly B. A. Mutagenesis of the DNA binding residues in bovine pancreatic DNase I: an investigation into the mechanism of sequence discrimination by a sequence selective nuclease. Nucl. Acids Res. 22:1991;6129-6132.
15. Doherty A. J., Worrall A. F., Connolly B. A. The roles of arginine 41 and tyrosine 76 in the coupling of DNA recognition to phosphodiester bond cleavage by DNaseI: a study using site directed mutagenesis. J. Mol. Biol. 251:1995;366-377.
16. Drew H. R., Travers A. A. DNA structural variations in the E. coli tyrT promoter. Cell. 37:1984;491-502.
17. Eaves G. N., Jeffries C. D. Isolation and properties of an exocellular nuclease of Serratia marcescens. J. Bacteriol. 85:1963;273-278.
18. Eisenstein M., Hope H., Haran T. E., Frolow F., Shakked Z., Rabinovich D. Low-temperature study of the A-DNA fragment d(GGGCGCCC). Acta Crystallog. 44:1988;625-628.
19. Filimonova M. N., Garusov A. V., Smetanina T. A., Andreeva M. A., Bogomolnaya L. M., Leshchinskaya I. B. Isoforms of Serratia nuclease: Comparative analysis of substrate specificity. Biochemistry (Moscow). 61:1996;1274-1278.
20. Flick K. E., Jurica M. S., Monnat R. J. Jr, Stoddard B. L. DNA binding and cleavage by the nuclear intron-encoded homing endonuclease I- Ppo I. Nature. 394:1998;96-101.
21. Franke I., Meiss G., Blecher D., Gimadutinow O., Urbanke C., Pingoud A. Genetic engeneering, production and characterisation of monomeric variants of the dimeric Serratia marcescens endonuclease. FEBS Letters. 425:1998;517-522.
22. Friedhoff P., Gimadutdinow O., Pingoud A. Identification of catalytically relevant amino acids of the extracellular Serratia marcescens endonuclease by alignment-guided mutagenesis. Nucl. Acids Res. 22:1994;3280-3287.
23. Friedhoff P., Kolmes B., Gimadutdinow O., Wende W., Krause K. L., Pingoud A. Analysis of the mechanism of the Serratia nuclease using site directed mutagenesis. Nucl. Acids Res. 24:1996a;2632-2639.
24. Friedhoff P., Meiss G., Kolmes B., Pieper U., Gimadutdinow O., Urbanke C., Pingoud A. Kinetic analysis of the cleavage of natural and synthetic substrates by the Serratia nuclease. Eur. J. Biochem. 241:1996b;572-580.
25. Friedhoff P., Franke I., Meiss G., Wende W., Krause K., Pingoud A. A similar active site for non-specific and specific endonucleases. Nature Struct. Biol. 6:1999a;112-113.
26. Friedhoff P., Franke I., Krause K-. L., Pingoud A. Cleavage experiments with deoxythymidine 3′-5′(p -nitrophenyl phosphate) suggest that the homing endonuclease I- Ppo I follows the same mechanism of phosphodiester bond hydrolysis as the non-specific Serratia nuclease. FEBS Letters. 443:1999b;209-214.
27. Gast F.-U., Kempe D., Spieker R. L., Sänger H. L. Secondary structure probing of potato spindle tuber viroid (PSTVd) and sequence comparison with other small pathogenic RNA replicons provides evidence form central non-canonical base-pairs, lare A-rich loops, and a terminal branch. J. Mol. Biol. 262:1996;652-670.
28. Gyi J. I., Conn G. L., Lane A. N., Brown T. Comparison of the thermodynamic stabilities and solution conformations of DNA/RNA hybrids containing purine-rich and pyrimidine-rich strands with DNA and RNA duplexes. Biochemistry. 35:1996;12538-12548.
29. Heinemann U., Lauble H., Frank R., Blöcker H. Crystal structure analysis of an A-DNA fragment at 1.8 A resolution: d(GCCCGGGC). Nucl. Acids Res. 15:1987;9531-9550.
30. Heinemann U., Rudolph L. N., Alings C., Morr M., Heikens W., Frank R., Blöcker H. Effect of a single 3′-methylene phosphonate linkage on the conformation of an A-DNA octamer double helix. Nucl. Acids Res. 19:1991;427-433.
31. Heinemann U., Alings C., Hahn M. Crystallographic studies of DNA helix structure. Biophys. Chem. 50:1994;157-167.
32. Herrera J. E., Chairs J. B. Characterization of preferred deoxyribonuclease I cleavage sites. J. Mol. Biol. 236:1994;405-411.
33. Hogan M. E., Roberson M. W., Austin R. H. DNA flexibility variation may dominate DNase I cleavage. Proc. Natl Acad. Sci. USA. 86:1989;9273-9277.
34. Holbrook S. R., Kim S-H. RNA crystallography. Biopolymers. 44:1997;3-21.
35. Jaeger J. A., Turner D. H., Zuker M. Improved predictions of secondary structures for RNA. Proc. Natl Acad. Sci. USA. 86:1989;7706-7710.
36. 2. Eur. J. Biochem. 152:1985;157-166.
37. Kolmes B., Franke I., Friedhoff P., Pingoud A. Analysis of the reaction mechanism of the non-specific endonuclease of Serratia marcescens using an artificial substrate. FEBS Letters. 397:1996;343-346.
38. Kunitz M. Crystalline deoxyribonuclease I. Isolation and general properties. Spectrophotometric method for the measurement of desoxyribonuclease activity. J. Gen. Physiol. 33:1950;349-362.
39. Leshchinskaya I. B., Balaban N. P., Egorova G. I., Tanyashin V. I., Tret'yak T. I. Isolation and characteristics of highly purified nuclease from Serratia marcescens. Biokhimiya. 39:1974;116-122.
40. Lowe M. J., Shellman J. A. Solvent effects on dinucleotide conformation. J. Mol. Biol. 65:1972;91-109.
41. Lunin V. Yu., Levdikov V. M., Shlyapnikov S. V., Blagova E. V., Lunin V. V., Wilson K. S., Mikhailov A. M. Three-dimensional structure of Serratia marcescens nuclease at 1.7 Å resolution and mechanism of its action. FEBS Letters. 412:1997;217-222.
42. Meiss G., Friedhoff P., Hahn M., Gimadutdinow O., Pingoud A. Sequence preferences in cleavage of dsDNA and ssDNA by the extracellular Serratia marcescens endonuclease. Biochemistry. 34:1995;11979-11988.
43. Meiss G., Franke I., Gimadutdinow O., Urbanke C., Pingoud A. Biochemical characterization of Anabaena sp. strain PCC 7120 non-specific nuclease NucA and its inhibitor NuiA. Eur. J. Biochem. 251:1998;924-934.
44. Miller M. D., Krause K. L. Identification of the Serratia endonuclease dimer: structural basis and implications for catalysis. Protein Sci. 5:1996;24-33.
45. Miller M. D., Tanner J., Alpaugh M., Benedik M. J., Krause K. L. 2.1 Å structure of Serratia endonuclease suggests a mechanism for binding to double-stranded DNA. Nature Struct. Biol. 1:1994;461-468.
46. Muro-Pastor A. M., Flores E., Herrero A., Wolk C. P. Identification, genetic analysis and characterization of a sugar-non-specific nuclease from the cyanobacteriumAnabaena sp. strain PCC 7120. Mol. Microbiol. 6:1992;3021-3030.
47. Nestle M., Roberts W. K. An extracellular nuclease from Serratia marcescens. I. Purification and some properties of the enzyme. J. Biol. Chem. 244:1969a;5213-5218.
48. Nestle M., Roberts W. K. An extracellular nuclease from Serratia marcescens. II. Specificity of the enzyme. J. Biol. Chem. 244:1969b;5219-5225.
49. Olson W. K. The spatial configuration of ordered polynucleotide chains. II. The poly r(A) helix. Nucl. Acids Res. 2:1975;2055-2068.
50. Olsthoorn C. S. M., Bostelaar L. J., van Boom J. H., Altona C. Conformational characteristics of the trinucleoside diphosphate dApdApdA and its constituents from nuclear magnetic resonance and circular dichroism studies. Eur. J. Biochem. 112:1980;95-110.
51. Prive G. G., Yanagi K., Dickerson R. E. Structure of the B -DNA decamer CCAACGTTGG and comparison with isomorphous decamers CCAAGATTGG and CCAGGCCTGG. J. Mol. Biol. 217:1991;177-199.
52. Ruiz-Carrillo A., Côté J. Primers for mitochondrial DNA replication generated by endonuclease G. Science. 261:1993;765-769.
53. Saenger W., Riecke J., Suck D. A structural model for the polyadenylic acid single helix. J. Mol. Biol. 93:1975;529-534.
54. Schumann G., Cannon K., Ma W. P., Crouch R. J., Boeke J. D. Antiretroviral effect of a gag-RNaseHI fusion gene. Gene Ther. 4:1997;593-599.
55. Shatzky-Schwartz M., Arbuckle N. D., Eisenstein M., Rabinovich D., Bareket-Samish A., Haran T. E., Luisi B. F., Shakked Z. X-ray and solution studies of DNA oligomers and implications for the structural basis of A-tract-dependent curvature. J. Mol. Biol. 267:1997;595-623.
56. Wahl M. C., Sundaralingam M. Crystal structures of A -DNA duplexes. Biopolymers. 44:1997;45-63.
57. Wang Y., Thomas G. A., Peticolas W. L. Sequence dependent conformations of oligomeric DNAs in aqueous solutions and in crystals. J. Biomol. Struct. Dynam. 5:1987;249-274.
58. Warren M. A., Steven J. E., Connolly B. A. Effects of non-conservative changes to tyrosine 76, a key DNA binding residue of DNaseI, on phosphodiester bond cleavage and DNA hydrolysis selectivity. Protein Eng. 10:1997;279-283.
59. 2complex at 2.3 Å resolution. J. Mol. Biol. 226:1992;1237-1256.
60. Wimberly B., Varani G., Tinoco I. Jr. The conformation of loop E of eukaryotic 5 S ribosomal RNA. Biochemistry. 32:1993;1078-1087.
61. Yonemura K., Matsumoto K., Maeda H. Isolation and characterization of nucleases from a clinical isolate of Serratia marcescens kums 3958. J. Biochem. (Tokyo). 93:1983;1287-1295.
62. 2: wrinkled D structure of the TATA moiety. Biochemistry. 26:1987;7905-7913.
63. 2: an analysis of vicinal proton-proton coupling constants from two-dimensional proton nuclear magnetic resonance. Biochemistry. 27:1988;6013-6020.
64. Zuker M. Computer prediction of RNA structure. Methods Enzymol. 180:1989;262-288.