Biophysical analysis of Thermus aquaticus single-stranded DNA binding protein

Biophysical Journal

Volumn 94, Issue 6, 2008, Pages 2269-2279

  Witte, Gregor ^a,b   Fedorov, Roman ^a   Curth, Ute ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; BACTERIAL PROTEIN; DNA BINDING PROTEIN; DNA DIRECTED DNA POLYMERASE GAMMA;

ARTICLE; BIOPHYSICS; CHEMISTRY; CRYSTALLIZATION; ESCHERICHIA COLI; HYDROGEN BOND; KINETICS; METABOLISM; METHODOLOGY; MUTATION; PROTEIN BINDING; SPECTROFLUOROMETRY; THERMUS; ULTRACENTRIFUGATION; X RAY CRYSTALLOGRAPHY;

ARGININE; BACTERIAL PROTEINS; BIOPHYSICS; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; DNA POLYMERASE III; DNA-BINDING PROTEINS; ESCHERICHIA COLI; HYDROGEN BONDING; KINETICS; MUTATION; PROTEIN BINDING; SPECTROMETRY, FLUORESCENCE; THERMUS; ULTRACENTRIFUGATION;

EID: 44049102511     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.121533     Document Type: Article

References (53)

1. Swamynathan, S. K., A. Nambiar, and R. V. Guntaka. 1998. Role of single-stranded DNA regions and Y-box proteins in transcriptional regulation of viral and cellular genes. FASEB J. 12:515-522.
2. Suck, D. 1997. Common fold, common function, common origin? Nat. Struct. Biol. 4:161-165.
3. Shamoo, Y., A. M. Friedman, M. R. Parsons, W. H. Konigsberg, and T. A. Steitz. 1995. Crystal structure of a replication fork single-stranded DNA binding protein (T4 gp32) complexed to DNA. Nature. 376:362-366.
4. Tucker, P. A., D. Tsernoglou, A. D. Tucker, F. E. Coenjaerts, H. Leenders, and P. C. van der Vliet. 1994. Crystal structure of the adenovirus DNA binding protein reveals a hook-on model for cooperative DNA binding. EMBO J. 13:2994-3002.
5. Folkers, P. J. M., M. Nilges, R. H. A. Folmer, R. N. H. Konings, and C. W. Hilbers. 1994. The solution structure of the Tyr41 - His mutant of the single- stranded DNA binding protein encoded by gene V of the filamentous bacteriophage M13. J. Mol. Biol. 236:229-246.
6. Skinner, M. M., H. Zhang, D. H. Leschnitzer, Y. Guan, H. Bellamy, R. M. Sweet, C. W. Gray, R. N. H. Konings, A. H.-J. Wang, and T. C. Terwilliger. 1994. Structure of the gene V protein of bacteriophage f1 determined by multiwavelength x-ray diffraction on the selenome-thionyl protein. Proc. Natl. Acad. Sci. USA. 91:2071-2075.
7. Curth, U., C. Urbanke, J. Greipel, H. Gerberding, V. Tiranti, and M. Zeviani. 1994. Single-stranded-DNA-binding proteins from human mitochondria and Escherichia coli have analogous physicochemical properties. Eur. J. Biochem. 221:435-443.
8. Greipel, J., C. Urbanke, and G. Maass. 1989. The single-stranded DNA binding protein of Escherichia coli: physicochemical properties and biologic functions. In Protein-Nucleic Acid Interaction. W. Saenger and U. Heinemann, editors. Macmillan, London. 61-86.
9. Lohman, T. M., and W. Bujalowski. 1990. E. coli single strand binding protein: multiple single stranded DNA binding modes and cooperativities. In The Biology of Nonspecific Protein DNA Interactions. A. Revzin, editor. CRC Press, Boca Raton, FL. 131-168.
10. Iftode, C., Y. Daniely, and J. A. Borowiec. 1999. Replication protein A(RPA): the eukaryotic SSB. Crit. Rev. Biochem. Mol. Biol. 34:141-180.
11. Dabrowski, S., M. Olszewski, R. Piatek, A. Brillowska-Dabrowska, G. Konopa, and J. Kur. 2002. Identification and characterization of single-stranded-DNA-binding proteins from Thermus thermophilus and Thermus aquaticus-new arrangement of binding domains. Microbiology. 148:3307-3315.
12. Eggington, J. M., N. Haruta, E. A. Wood, and M. M. Cox. 2004. The single-stranded DNA-binding protein of Deinococcus radiodurans. BMC Microbiol. 4:2.
13. Witte, G., C. Urbanke, and U. Curth. 2005. Single-stranded DNA-binding protein of Deinococcus radiodurans: a biophysical characterization. Nucleic Acids Res. 33:1662-1670.
14. Fedorov, R., G. Witte, C. Urbanke, D. J. Manstein, and U. Curth. 2006. 3D structure of Thermus aquaticus single-stranded DNA-binding protein gives insight into the functioning of SSB proteins. Nucleic Acids Res. 34:6708-6717.
15. Jedrzejczak, R., M. Dauter, Z. Dauter, M. Olszewski, A. Dlugolecka, and J. Kur. 2006. Structure of the single-stranded DNA-binding protein SSB from Thermus aquaticus. Acta Crystallogr. D: Biol. Crystallogr. 62:1407-1412.
16. Curth, U., J. Genschel, C. Urbanke, and J. Greipel. 1996. In vitro and in vivo function of the C-terminus of Escherichia coli single-stranded DNA binding protein. Nucleic Acids Res. 24:2706-2711.
17. Cadman, C. J., and P. McGlynn. 2004. PriA helicase and SSB interact physically and functionally. Nucleic Acids Res. 32:6378-6387.
18. Handa, P., N. Acharya, and U. Varshney. 2001. Chimeras between single-stranded DNA-binding proteins from Escherichia coli and Mycobacterium tuberculosis reveal that their C-terminal domains interact with uracil DNA glycosylases. J. Biol. Chem. 276:16992-16997.
19. Kelman, Z., A. Yuzhakov, J. Andjelkovic, and M. O'Donnell. 1998. Devoted to the lagging strand-the subunit of DNA polymerase III holoenzyme contacts SSB to promote processive elongation and sliding clamp assembly. EMBO J. 17:2436-2449.
20. Witte, G., C. Urbanke, and U. Curth. 2003. DNA polymerase III chi subunit ties single-stranded DNA binding protein to the bacterial replication machinery. Nucleic Acids Res. 31:4434-4440.
21. McGhee, J. D., and P. H. Von Hippel. 1974. Theoretical aspects of DNA-protein interactions: co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice. J. Mol. Biol. 86:469-489.
22. Schwarz, G., and F. Watanabe. 1983. Thermodynamics and kinetics of co-operative protein-nucleic acid binding. I. General aspects of analysis of data. J. Mol. Biol. 163:467-484.
23. Greipel, J., G. Maass, and F. Mayer. 1987. Complexes of the single-stranded DNA-binding protein from Escherichia coli (Eco SSB) with poly(dT). An investigation of their structure and internal dynamics by means of electron microscopy and NMR. Biophys. Chem. 26:149-161.
24. Lohman, T. M., L. B. Overman, and S. Datta. 1986. Salt-dependent changes in the DNA binding co-operativity of Escherichia coli single strand binding protein. J. Mol. Biol. 187:603-615.
25. Raghunathan, S., A. G. Kozlov, T. M. Lohman, and G. Waksman. 2000. Structure of the DNA binding domain of E. coli SSB bound to ssDNA. Nat. Struct. Biol. 7:648-652.
26. Raghunathan, S., C. S. Ricard, T. M. Lohman, and G. Waksman. 1997. Crystal structure of the homo-tetrameric DNA binding domain of Escherichia coli single-stranded DNA-binding protein determined by multiwavelength x-ray diffraction on the selenomethionyl protein at 2.9-Å resolution. Proc. Natl. Acad. Sci. USA. 94:6652-6657.
27. Urbanke, C., and A. Schaper. 1990. Kinetics of binding of single-stranded DNA binding protein from Escherichia coli to single-stranded nucleic acids. Biochemistry. 29:1744-1749.
28. Kowalczykowski, S. C., N. Lonberg, J. W. Newport, and P. H. VonHippel. 1981. Interactions of bacteriophage T4-coded gene 32 protein with nucleic acids. J. Mol. Biol. 145:75-104.
29. Pace, C. N., F. Vajdos, L. Fee, G. Grimsley, and T. Gray. 1995. How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4:2411-2423.
30. Lohman, T. M., and L. B. Overman. 1985. Two binding modes in Escherichia coli single strand binding protein-single stranded DNA complexes. Modulation by NaCl concentration. J. Biol. Chem. 260: 3594-3603.
31. Bayer, I., A. Fliess, J. Greipel, C. Urbanke, and G. Maass. 1989. Modulation of the affinity of the single-stranded DNA-binding protein of Escherichia coli (E. coli SSB) to poly(dT) by site-directed mutagenesis. Eur. J. Biochem. 179:399-404.
32. Landwehr, M., U. Curth, and C. Urbanke. 2002. A dimeric mutant of the homotetrameric single-stranded DNA binding protein from Escherichia coli. Biol. Chem. 383:1325-1333.
33. L control. Biochemistry. 25:21-25.
34. Curth, U., J. Greipel, C. Urbanke, and G. Maass. 1993. Multiple binding modes of the single-stranded DNA binding protein from Escherichia coli as detected by tryptophan fluorescence and sitedirected mutagenesis. Biochemistry. 32:2585-2591.
35. Curth, U., I. Bayer, J. Greipel, F. Mayer, C. Urbanke, and G. Maass. 1991. Amino acid 55 plays a central role in tetramerization and function of Escherichia coli single-stranded DNA binding protein. Eur. J. Biochem. 196:87-93.
36. Kindler, B. 1997. AKKUPROG: Evaluation of chemical reaction kinetics and analysis of biopolymers using ultracentrifugation. Application to protein-DNA interactions. PhD thesis. Universitat Hannover, Hanover, Germany.
37. Schuck, P. 2000. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys. J. 78:1606-1619.
38. Dam, J., and P. Schuck. 2005. Sedimentation velocity analysis of heterogeneous protein-protein interactions: sedimentation coefficient distributions c(s) and asymptotic boundary profiles from GilbertJenkins theory. Biophys. J. 89:651-666.
39. Urbanke, C., G. Witte, and U. Curth. 2005. Sedimentation velocity method in the analytical ultracentrifuge for the study of protein-protein interactions. Methods Mol. Biol. 305:101-114.
40. Gralén, N., and G. Lagermalm. 1952. A contribution to the knowledge of some physico-chemical properties of polystyrene. J. Phys. Chem. 56:514-523.
41. Lamm, O. 1929. Die Differentialgleichung der Ultrazentrifugierung. Arkiv Matematik Astronomi Fysik. 21B:1-1-.
42. Durchschlag, H. 1986. Specific volumes of biological macromolecules and some other molecules of biological interest. In Thermodynamic Data for Biochemistry and Biotechnology. H. Hinz, editor. Springer, Berlin/Heidelberg. 45-128.
43. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
44. Lebowitz, J., M. S. Lewis, and P. Schuck. 2002. Modern analytical ultracentrifugation in protein science: a tutorial review. Protein Sci. 11:2067-2079.
45. Eggington, J. M., A. G. Kozlov, M. M. Cox, and T. M. Lohman. 2006. Polar destabilization of DNA duplexes with single-stranded overhangs by the Deinococcus radiodurans SSB protein. Biochemistry. 45:14490-14502.
46. Bujalowski, W., and T. M. Lohman. 1987. A general method of analysis of ligand-macromolecule equilibria using a spectroscopic signal from the ligand to monitor binding. Application to Escherichia coli single-strand binding protein-nucleic acid interactions. Biochemistry. 26:3099-3106.
47. Genschel, J., U. Curth, and C. Urbanke. 2000. Interaction of E. colisingle-stranded DNA binding protein (SSB) with exonuclease I. The carboxy-terminus of SSB is the recognition site for the nuclease. Biol. Chem. 381:183-192.
48. Dam, J., C. A. Velikovsky, R. A. Mariuzza, C. Urbanke, and P. Schuck. 2005. Sedimentation velocity analysis of heterogeneous protein-protein interactions: Lamm equation modeling and sedimentation coefficient distributions c(s). Biophys. J. 89:619-634.
49. Lohman, T. M., and M. E. Ferrari. 1994. Escherichia coli singlestranded DNA-binding protein: multiple DNA-binding modes and cooperativities. Annu. Rev. Biochem. 63:527-570.
50. Bernstein, D. A., J. M. Eggington, M. P. Killoran, A. M. Misic, M. M. Cox, and J. L. Keck. 2004. Crystal structure of the Deinococcus radiodurans single-stranded DNA-binding protein suggests a mechanism for coping with DNA damage. Proc. Natl. Acad. Sci. USA. 101:8575-8580.
51. Chase, J. W., J. J. L'ltalien, J. B. Murphy, E. K. Spicer, and K. R. Williams. 1984. Characterization of the E. coli ssb113 mutant singlestranded DNA binding protein. Cloning of the gene, DNA and protein sequence analysis, HPLC, peptide mapping and DNA binding studies. J. Biol. Chem. 259:805-814.
52. Williams, K. R., E. K. Spicer, M. B. Lopresti, R. A. Gugenheimer, and J. W. Chase. 1983. Limited proteolysis studies on the E. coli singlestranded DNA binding protein. J. Biol. Chem. 258:3346-3355.
53. Roy, R., A. G. Kozlov, T. M. Lohman, and T. Ha. 2007. Dynamic structural rearrangements between DNA binding modes of E. coli SSB protein. J. Mol. Biol. 369:1244-1257.