Functional analysis of the Streptomyces coelicolor NrdR ATP-cone domain: Role in nucleotide binding, oligomerization, and DNA interactions

Journal of Bacteriology

Volumn 191, Issue 4, 2009, Pages 1169-1179

  Grinberg, Inna ^a   Shteinberg, Tatyana ^a   Hassan, Quamrul ^b   Aharonowitz, Yair ^a   Borovok, Ilya ^a   Cohen, Gerald ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DEOXYADENOSINE TRIPHOSPHATE; MUTANT PROTEIN; RIBONUCLEOTIDE REDUCTASE; BACTERIAL DNA; BACTERIAL PROTEIN;

ARTICLE; ATP CONE DOMAIN; BACTERIAL GENE; BIOINFORMATICS; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DNA BINDING; GEL FILTRATION CHROMATOGRAPHY; GEL MOBILITY SHIFT ASSAY; MUTATION; NONHUMAN; NRDAB GENE; NRDJ GENE; OLIGOMERIZATION; OPERON; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SEQUENCE ANALYSIS; STREPTOMYCES COELICOLOR; WESTERN BLOTTING; WILD TYPE; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE;

BACTERIA (MICROORGANISMS); STREPTOMYCES; STREPTOMYCES COELICOLOR;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEOTIDE REDUCTASES; STREPTOMYCES COELICOLOR;

EID: 60849105356     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01145-08     Document Type: Article

References (49)

1. Aravind, L., Y. I. Wolf, and E. V. Koonin. 2000. The ATP-cone: an evolutionarily mobile, ATP-binding regulatory domain. J. Mol. Microbiol. Biotechnol. 2:191-194.
2. Augustin, L. B., B. A. Jacobson, and J. A. Fuchs. 1994. Escherichia coli Fis and DnaA proteins bind specifically to the nrd promoter region and affect expression of an nrd-lac fusion. J. Bacteriol. 176:378-387.
3. Beloin, C., S. McKenna, and C. J. Dorman. 2002. Molecular dissection of VirB, a key regulator of the virulence cascade of Shigella flexneri. J. Biol. Chem. 277:15333-15344.
4. Birgander, P. L., A. Kasrayan, and B. M. Sjoberg. 2004. Mutant R1 proteins from Escherichia coli class Ia ribonucleotide reductase with altered responses to dATP inhibition. J. Biol. Chem. 279:14496-14501.
5. Borovok, I., B. Gorovitz, M. Yanku, R. Schreiber, B. Gust, K. Chater, Y. Aharonowitz, and G. Cohen. 2004. Alternative oxygen-dependent and oxygen-independent ribonucleotide reductases in Streptomyces: cross-regulation and physiological role in response to oxygen limitation. Mol. Microbiol. 54:1022-1035.
6. Borovok, I., R. Kreisberg-Zakarin, M. Yanko, R. Schreiber, M. Myslovati, F. Aslund, A. Holmgren, G. Cohen, and Y. Aharonowitz. 2002. Streptomyces spp. contain class Ia and class II ribonucleotide reductases: expression analysis of the genes in vegetative growth. Microbiology 148:391-404.
7. Boston, T., and T. Atlung. 2003. FNR-mediated oxygen-responsive regulation of the nrdDG operon of Escherichia coli. J. Bacteriol. 185:5310-5313.
8. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
9. Brown, N. C., and P. Reichard. 1969. Ribonucleoside diphosphate reductase: formation of active and inactive complexes of proteins B1 and B2. J. Mol. Biol. 46 :25-38.
10. Chabes, A., and B. Stillman. 2007. Constitulively high dNTP concentration inhibits cell cycle progression and the DNA damage checkpoint in yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 104:1183-1188.
11. Chater, K. F. 1993. Genetics of differentiation in Streptomyces. Annu. Rev. Microbiol. 47:685-713.
12. de los Rios, S., and J. J. Perona. 2007. Structure of the Escherichia coli leucine-responsive regulatory protein Lrp reveals a novel octameric assembly. J. Mol. Biol. 366:1589-1602.
13. Eklund, H., U. Uhlin, M. Farnegardh, D. T. Logan, and P. Nordlund. 2001. Structure and function of the radical enzyme ribonucleotide reductase. Prog. Biophys. Mol. Biol. 77:177-268.
14. Eriksson, M., U. Uhlin, S. Ramaswamy, M. Ekberg, K. Regnstrom, B. M. Sjoberg, and H. Eklund. 1997. Binding of allosteric effectors to ribonucleotide reductase protein R1: reduction of active-site cysteines promotes substrate binding. Structure 5:1077-1092.
15. Gamier, J., J. F. Gibrat, and B. Robson. 1996. GOR method for predicting protein secondary structure from amino acid sequence. Methods Enzymol. 266:540-553.
16. Gon, S., and J. Beckwith. 2006. Ribonucleotide reductases: influence of environment on synthesis and activity. Antioxid. Redox Signal. 8:773-780.
17. Gon, S., J. E. Camara, H. K. Klungsoyr, E. Crooke, K. Skarstad, and J. Beckwith. 2006. A novel regulatory mechanism couples deoxyribonucleotide synthesis and DNA replication in Escherichia coli. EMBO J. 25: 1137-1147.
18. Grinberg, I., T. Shteinberg, B. Gorovitz, Y. Aharonowitz, G. Cohen, and I. Borovok. 2006. The Streptomyces NrdR transcriptional regulator is a Zn ribbon/ATP cone protein that binds to the promoter regions of class Ia and class II ribonucleotide reductase operons. J. Baeteriol. 188:7635-7644.
19. Guex, N., and M. C. Peitsch. 1997. SWISS-MODEL and the Swiss-Pdb-Viewer: an environment for comparative protein modeling. Electrophoresis 1 8:2714-2723.
20. Herrick, J., and B. Sclavi. 2007. Ribonucleotide reductase and the regulation of DNA replication: an old story and an ancient heritage. Mol. Microbiol. 63:22-34.
21. Higgins, D. G., J. D. Thompson, and T. J. Gibson. 1996. Using CLUSTAL for multiple sequence alignments. Methods Enzymol. 266:383-402.
22. Ingemarson, R., and L. Thelander. 1996. A kinetic study on the influence of nucleoside triphosphate effectors on subunit interaction in mouse ribonucleotide reductase. Biochemistry 35:8603-8609.
23. Jacobson, B. A., and J. A. Fuchs. 1998. A 45-bp inverted repeat is required for cell cycle regulation of the Escherichia coli nrd operon. Mol. Microbiol. 28:1307-1314.
24. Jacobson, B. A., and J. A. Fuchs. 1998. Multiple cis-acting sites positively regulate Escherichia coli nrd expression. Mol. Microbiol. 28:1315-1322.
25. Jordan, A., I. Gibert, and J. Barbe. 1995. Two different operons for the same function: comparison of the Salmonella typhimurium nrdAB and nrdEF genes. Gene 167:75-79.
26. Jordan, A., and P. Reichard. 1998. Ribonucleotide reductases. Annu. Rev. Biochem. 67:71-98.
27. Kashlan, O. B., and B. S. Cooperman. 2003. Comprehensive model for allosteric regulation of mammalian ribonucleotide reductase: refinements and consequences. Biochemistry 42:1696-1706.
28. Kashlan, O. B., C. P. Scott, J. D. Lear, and B. S. Cooperman. 2002. A comprehensive model for the allosteric regulation of mammalian ribonucleotide reductase. Functional consequences of ATP-and dATP-induced oligomerization of the large subunit. Biochemistry 41:462-474.
29. Kieser, T., M. J. Bibb, M. J. Buttner, K. F. Chater, and D. A. Hopwood. 2000. Practical Streptomyces genetics. John Innes Foundation, Norwich. United Kingdom.
30. Krishna, S. S., I. Majumdar, and N. V. Grishin. 2003. Structural classification of zinc fingers: survey and summary. Nucleic Acids Res. 31:532-550.
31. Kumar, J. K., S. Tabor, and C. C. Richardson. 2004. Proteomic analysis of thioredoxin-targeted proteins in Escherichia coli. Proc. Natl. Acad. Sci. USA 101:375937-375964.
32. Kumar, S., K. Tamura, and M. Nei. 2004. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 5:150-163.
33. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
34. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson, and D. G. Higgins. 2007. CLUSTAL W and CLUSTAL X version 2.0. Bioinformatics 23:2947-2948.
35. Mathews, C. K. 2006. DNA precursor metabolism and genomic stability. FASEB J. 20:1300-1314.
36. Nordlund, P., and P. Reichard. 2006. Ribonucleotide reductases. Annu. Rev. Biochem. 75:681-706.
37. Reichard, P. 1993. From RNA to DNA, why so many ribonucleotide reductases? Science 260:1773-1777.
38. Rodionov, D. A., and M. S. Gelfand. 2005. Identification of a bacterial regulatory system for ribonucleotide reductases by phylogenetic profiling. Trends Genet. 21:385-389.
39. Rofougaran, R., M. Vodnala, and A. Hofer. 2006. Enzymatically active mammalian ribonucleotide reductase exists primarily as an α6β2 octamer. J. Biol. Chem. 281:27705-27711.
40. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, NY.
41. Stubbe, J. 2000. Ribonucleotide reductases: the link between an RNA and a DNA world? Curr. Opin. Struct. Biol. 10:731-736.
42. Sun, L., and J. A. Fuchs. 1992. Escherichia coli ribonucleotide reductase expression is cell cycle regulated. Mol. Biol. Cell 3:1095-1105.
43. Sun, X., J. Harder, M. Krook, H. Jornvall, B. M. Sjoberg, and P. Reichard. 1993. A possible glycine radical in anaerobic ribonucleotide reductase from Escherichia coli: nucleotide sequence of the cloned nrdD gene. Proc. Natl. Acad. Sci. USA 90:577-581.
44. Thelander, L. 1973. Physicochemical characterization of ribonucleoside diphosphate reductase from Escherichia coli. J. Biol. Chem. 248:4591-4601.
45. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
46. Torrents, E., I. Grinberg, B. Gorovitz-Harris, H. Lundstrom, I. Borovok, Y. Aharonowitz, B. M. Sjoberg, and G. Cohen. 2007. NrdR controls differential expression of the Escherichia coli ribonucleotide reductase genes. J. Bacteriol. 189:5012-5021.
47. Torrents, E., M. Westman, M. Sahlin, and B. M. Sjoberg. 2006. Ribonucleotide reductase modularity: atypical duplication of the ATP-cone domain in Pseudomonas aeruginosa. J. Biol. Chem. 281:25287-25296.
48. Uhlin, U., and H. Eklund. 1994. Structure of ribonucleotide reductase protein R1. Nature 370:533-539.
49. Wheeler, L. J., I. Rajagopal, and C. K. Mathews. 2005. Stimulation of mutagenesis by proportional deoxyribonucleoside triphosphate accumulation in Escherichia coli. DNA Repair 4:1450-1456.