Structural Studies on the Second Mycobacterium smegmatis Dps: Invariant and Variable Features of Structure, Assembly and Function

Journal of Molecular Biology

Volumn 375, Issue 4, 2008, Pages 948-959

  Roy, Siddhartha ^a   Saraswathi, Ramachandran ^a   Chatterji, Dipankar ^a   Vijayan, M ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

assembly; cubic close packing; DNA binding protein; ferroxidation

Indexed keywords

DNA BINDING PROTEIN; DPS PROTEIN; PROTEIN DPS1; PROTEIN DPS2; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; BACTERIAL GENOME; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CRYSTAL STRUCTURE; MOLECULAR CLONING; MYCOBACTERIUM SMEGMATIS; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN STABILITY; PROTEIN STRUCTURE;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM SMEGMATIS;

EID: 37349040333     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.10.023     Document Type: Article

References (53)

1. Kolter R., Siegele D.A., and Tormo A. The stationary phase of the bacterial life cycle. Annu. Rev. Microbiol. 47 (1993) 855-874
2. Almiron M., Link A.J., Furlong D., and Kolter R. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 6 (1992) 2646-2654
3. Azam A.T., Iwata A., Nishimura A., Ueda S., and Ishihama A. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol. 181 (1999) 6361-6370
4. Zhao G., Ceci P., Ilari A., Giangiacomo L., Laue T.M., Chiancone E., and Chasteen N.D. Iron and hydrogen peroxide detoxification properties of DNA-binding protein from starved cells. A ferritin-like DNA-binding protein of Escherichia coli. J. Biol. Chem. 277 (2002) 27689-27696
5. 2+ derivatives. J. Mol. Biol. 307 (2001) 587-603
6. Carrondo M.A. Ferritins, iron uptake and storage from the bacterioferritin viewpoint. EMBO J. 22 (2003) 1959-1968
7. Brentjens R.J., Ketterer M., Apicella M.A., and Spinola S.M. Fine tangled pili expressed by Haemophilus ducreyi are a novel class of pili. J. Bacteriol. 178 (1996) 808-816
8. Nicodeme M., Perrin C., Hols P., Bracquart P., and Gaillard J.L. Identification of an iron-binding protein of the Dps family expressed by Streptococcus thermophilus. Curr. Microbiol. 48 (2004) 51-56
9. Cooksley C., Jenks P.J., Green A., Cockayne A., Logan R.P., and Hardie K.R. NapA protects Helicobacter pylori from oxidative stress damage, and its production is influenced by the ferric uptake regulator. J. Med. Microbiol. 52 (2003) 461-469
10. Zanotti G., Papinutto E., Dundon W.G., Battistutta R., Seveso M., DelGiudice G., et al. Structure of the neutrophil-activating protein from Helicobacter pylori. J. Mol. Biol. 323 (2002) 125-130
11. Thumiger A., Polenghi A., Papinutto E., Battistutta R., Montecucco C., and Zanotti G. Crystal structure of antigen TpF1 from Treponema pallidum. Proteins 62 (2006) 827-830
12. Li X., Pal U., Ramamoorthi N., Liu X., Desrosiers D.C., Eggers C.H., et al. The Lyme disease agent Borrelia burgdorferi requires BB0690, a Dps homologue, to persist within ticks. Mol. Microbiol. 63 (2007) 694-710
13. Ferguson G.P., Creighton R.I., Nikolaev Y., and Booth I.R. Importance of RpoS and Dps in survival of exposure of both exponential- and stationary-phase Escherichia coli cells to the electrophile N-ethylmaleimide. J. Bacteriol. 180 (1998) 1030-1036
14. Choi S.H., Baumler D.J., and Kaspar C.W. Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157:H7. Appl. Environ. Microbiol. 66 (2000) 3911-3916
15. Nair S., and Finkel S.E. Dps protects cells against multiple stresses during stationary phase. J. Bacteriol. 186 (2004) 4192-4198
16. Papinutto E., Dundon W.G., Pitulis N., Battistutta R., Montecucco C., and Zanotti G. Structure of two iron binding proteins from Bacillus anthracis. J. Biol. Chem. 277 (2002) 15093-15098
17. Liu X., Kim K., Leighton T., and Theil E.C. Paired Bacillus anthracis Dps (mini-ferritin) have different reactivities with peroxide. J. Biol. Chem. 281 (2006) 27827-27835
18. Antelmann H., Engelmann S., Schmid R., Sorokin A., Lapidus A., and Hecker M. Expression of a stress- and starvation-induced dps/pexB-homologous gene is controlled by the alternative sigma factor sigmaB in Bacillus subtilis. J. Bacteriol. 179 (1997) 7251-7256
19. Chen L., and Helmann J.D. Bacillus subtilis MrgA is a Dps(PexB) homologue: evidence for metalloregulation of an oxidative-stress gene. Mol. Microbiol. 18 (1995) 295-300
20. Romão C.V., Mitchell E.P., and McSweeney S. The crystal structure of Deinococcus radiodurans Dps protein (DR2263) reveals the presence of a novel metal centre in the N terminus. J. Biol. Inorg. Chem. 11 (2006) 891-902
21. Kim S.G., Bhattacharyya G., Grove A., and Lee Y.H. Crystal structure of Dps-1, a functionally distinct Dps protein from Deinococcus radiodurans. J. Mol. Biol. 361 (2006) 105-114
22. Cuypers M.G., Mitchell E.P., Romao C.V., and McSweeney S.M. The crystal structure of the Dps2 from Deinococcus radiodurans reveals an unusual pore profile with a non-specific metal binding site. J. Mol. Biol. 371 (2007) 787-799
23. Gupta S., Pandit S.B., Srinivasan N., and Chatterji D. Proteomics analysis of carbon-starved Mycobacterium smegmatis: induction of Dps-like protein. Protein Eng. 15 (2002) 503-512
24. Gupta S., and Chatterji D. Bimodal protection of DNA by Mycobacterium smegmatis DNA-binding protein from stationary phase cells. J. Biol. Chem. 278 (2003) 5235-5241
25. Roy S., Gupta S., Das S., Sekar K., Chatterji D., and Vijayan M. X-ray analysis of Mycobacterium smegmatis Dps and a comparative study involving other Dps-like molecules. J. Mol. Biol. 18 (2004) 1103-1113
26. Chowdhury R.P., and Chatterji D. Estimation of Förster's distance between two ends of Dps protein from Mycobacteria: distance heterogeneity as a function of oligomerization and DNA binding. Biophys. Chem. 128 (2007) 19-29
27. Roy S., Saraswathi R., Gupta S., Sekar K., Chatterji D., and Vijayan M. Role of N and C-terminal tails in DNA binding and assembly in Dps: structural studies of Mycobacterium smegmatis Dps deletion mutants. J. Mol. Biol. 370 (2007) 752-767
28. Peterson J.D., Umayam L.A., Dickinson T.M., Hickey E.K., and White O. The comprehensive microbial resource. Nucleic Acids Res. 29 (2001) 123-125
29. Stillman T.J., Upadhyay M., Norte V.A., Sedelnikova S.E., Carradus M., et al. The crystal structures of Lactococcus lactis MG1363 Dps proteins reveal the presence of an N-terminal helix that is required for DNA binding. Mol. Microbiol. 57 (2005) 1101-1112
30. Grant R.A., Filman D.J., Finkel S.E., Kolter R., and Hogle J.M. The crystal structure of Dps, a ferritin homolog that binds and protects DNA. Nat. Struct. Biol. 5 (1998) 294-303
31. Ilari A., Stefanini S., Chiancone E., and Tsernoglou D. The dodecameric ferritin from Listeria innocua contains a novel intersubunit iron-binding site. Nat. Struct. Biol. 7 (2000) 38-43
32. Ren B., Tibbelin G., Kajino T., Asami O., and Ladenstein R. The multi-layered structure of Dps with a novel di-nuclear ferroxidase centre. J. Mol. Biol. 6 (2003) 467-477
33. Ceci P., Ilari A., Falvo E., and Chiancone E. The Dps protein of Agrobacterium tumefaciens does not bind to DNA but protects it toward oxidative cleavage: X-ray crystal structure, iron binding, and hydroxyl-radical scavenging properties. J. Biol. Chem. 278 (2003) 20319-20326
34. Zeth K., Offermann S., Essen L.O., and Oesterhelt D. Iron-oxo clusters biomineralizing on protein surfaces: structural analysis of Halobacterium salinarum DpsA in its low- and high-iron states. Proc. Natl. Acad. Sci. USA 101 (2004) 13780-13785
35. Franceschini S., Ceci P., Alaleona F., Chiancone E., and Ilari A. Antioxidant Dps protein from the thermophilic cyanobacterium Thermosynechococcus elongatus. FEBS J. 273 (2006) 4913-4928
36. Kauko A., Haataja S., Pulliainen A.T., Finne J., and Papageorgiou A.C. Crystal structure of Streptococcus suis Dps-like peroxide resistance protein Dpr: implications for iron incorporation. J. Mol. Biol. 338 (2004) 547-558
37. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215 (1990) 403-410
38. Raghunathan S., Kozlov A.G., Lohman T.M., and Waksman G. Structure of the DNA binding domain of E. coli SSB bound to SSDNA. Nat. Struct. Biol. 7 (2000) 648-652
39. Yang C., Curth U., Urbanke C., and Kang C. Crystal structure of human mitochondrial single-stranded DNA binding protein at 2.4 Å resolution. Nat. Struct. Biol. 4 (1997) 153-157
40. Matsumoto T., Morimoto Y., Shibata N., Kinebuchi T., Shimamoto N., Tsukihara T., and Yasuoka N. Roles of functional loops and the C-terminal segment of a single-stranded DNA binding protein elucidated by X-ray structure analysis. J. Biochem. 127 (2000) 329-335
41. Saikrishnan K., Jeyakanthan J., Venkatesh J., Acharya N., Sekar K., Varshney U., and Vijayan M. Structure of Mycobacterium tuberculosis single-stranded DNA-binding protein. Variability in quaternary structure and its implications. J. Mol. Biol. 331 (2003) 385-393
42. Luger K., Mader A.W., Richmond R.K., Sargent D.F., and Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389 (1997) 251-260
43. Wolf S.G., Frenkiel D., Arad T., Finkel S.E., Kolter R., and Minsky A. DNA protection by stress-induced biocrystallization. Nature 400 (1999) 83-85
44. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
45. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
46. Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 (1994) 760-763
47. Storoni L.C., McCoy A.J., and Read R.J. Likelihood enhanced fast rotation functions. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 432-438
48. Higgins D., Thompson J., Gibson T., Thompson J.D., Higgins D.G., and Gibson T.J. 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 (1994) 4673-4680
49. Brunger A.T., Adams P.D., Clore G.M., Delano W.L., Gross P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 (1998) 905-921
50. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2126-2132
51. Laskowski R.A., Moss D.S., and Thornton J.M. Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 231 (1993) 1049-1067
52. Cohen G.E. ALIGN: a program to superimpose protein coordinates, accounting for insertions and deletions. J. Appl. Crystallogr. 30 (1997) 1160-1161
53. McDonald I.K., and Thornton J.M. Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238 (1994) 777-793