Bound or free: Interaction of the C-terminal domain of escherichia coli single-stranded DNA-binding protein (SSB) with the tetrameric core of SSB

Biochemistry

Volumn 53, Issue 12, 2014, Pages 1925-1934

  Su, Xun Cheng ^a,b   Wang, Yao ^c   Yagi, Hiromasa ^b   Shishmarev, Dmitry ^b   Mason, Claire E ^c   Smith, Paul J ^b   Vandevenne, Marylène ^d   Dixon, Nicholas E ^b,c   Otting, Gottfried ^b  

^a NANKAI UNIVERSITY   (China)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^c UNIVERSITY OF WOLLONGONG   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; DNA; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTROSTATICS; ESCHERICHIA COLI; OLIGOMERS; REPAIR;

C-TERMINAL SEGMENTS; ELECTRON PARAMAGNETIC RESONANCE SPECTROSCOPY; ELECTROSTATIC EFFECT; HIGH MOLECULAR MASS; INTRAMOLECULAR BINDING; NUCLEAR MAGNETIC RESONANCE(NMR); SINGLE-STRANDED DNA; SINGLE-STRANDED DNA-BINDING PROTEINS;

PEPTIDES;

C PEPTIDE; GLUTAMATE POTASSIUM; METHIONINE; NITROGEN 15; SINGLE STRANDED DNA BINDING PROTEIN; TETRAMER;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; C TERMINAL DOMAIN; DISSOCIATION CONSTANT; DNA REPLICATION; ELECTRON SPIN RESONANCE; ESCHERICHIA COLI; FREQUENCY MODULATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; IONIC STRENGTH; MOLECULAR WEIGHT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE; STATIC ELECTRICITY; TITRIMETRY;

AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; ESCHERICHIA COLI PROTEINS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; STATIC ELECTRICITY;

EID: 84898080409     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi5001867     Document Type: Article

References (40)

1. Shereda, R. D., Kozlov, A. G., Lohman, T. M., Cox, M. M., and Keck, J. L. (2008) SSB as an organizer/mobilizer of genome maintenance complexes Crit. Rev. Biochem. Mol. Biol. 43, 289-318
2. Marceau, A. H. (2012) Functions of single-strand DNA-binding proteins in DNA replication, recombination and repair Methods Mol. Biol. 922, 1-21
3. Meyer, R. R. and Laine, P. S. (1990) The single-stranded DNA-binding protein of Escherichia coli Microbiol. Rev. 54, 342-380
4. Lohman, T. M. and Ferrari, M. E. (1994) Escherichia coli single-stranded DNA-binding protein: Multiple DNA-binding modes and cooperativities Annu. Rev. Biochem. 63, 527-570
5. Suck, D. (1997) Common fold, common function, common origin? Nat. Struct. Biol. 4, 161-165
6. Bujalowski, W., Overman, L. B., and Lohman, T. M. (1988) Binding mode transitions of Escherichia coli single strand binding protein-single-stranded DNA complexes. Cation, anion, pH, and binding density effects J. Biol. Chem. 263, 4629-4640
7. Overman, L. B. and Lohman, T. M. (1994) Linkage of pH, anion and cation effects in protein-nucleic acid equilibria. Escherichia coli SSB protein-single stranded nucleic acid interactions J. Mol. Biol. 236, 165-178
8. Williams, K. R., Spicer, E. K., LoPresti, M. B., Guggenheimer, R. A., and Chase, J. W. (1983) Limited proteolysis studies on the Escherichia coli single-stranded DNA binding protein. Evidence for a functionally homologous domain in both the Escherichia coli and T4 DNA binding proteins J. Biol. Chem. 258, 3346-3355
9. Mason, C. E., Jergic, S., Lo, A. T. Y., Wang, Y., Dixon, N. E., and Beck, J. L. (2013) Escherichia coli single-stranded DNA-binding protein: NanoESI-MS studies of salt-modulated subunit exchange and DNA binding transactions J. Am. Soc. Mass Spectrom. 24, 274-285
10. 56 DNA binding modes Biochemistry 27, 2260-2265
11. Yang, C., Curth, U., Urbanke, C., and Kang, C. H. (1997) Crystal structure of human mitochondrial single-stranded DNA binding protein at 2.4 Å resolution Nat. Struct. Biol. 4, 153-157
12. Raghunathan, S., Ricard, C. S., Lohman, T. M., and Waksman, G. (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. U.S.A. 94, 6652-6657
13. Raghunathan, S., Kozlov, A. G., Lohman, T. M., and Waksman, G. (2000) Structure of the DNA binding domain of E. coli SSB bound to ssDNA Nat. Struct. Biol. 7, 648-652
14. Matsumoto, T., Morimoto, Y., Shibata, N., Kinebuchi, T., Shimamoto, N., Tsukihara, T., and Yasuoka, N. (2000) Roles of functional loops and C-terminal segments of a single-stranded DNA binding protein elucidated by X-ray structural analysis J. Biochem. 127, 329-335
15. Savvides, S. N., Raghunathan, S., Fütterer, K., Kozlov, A. G., Lohman, T. M., and Waksman, G. (2004) The C-terminal domain of full-length E. coli SSB is disordered even when bound to DNA Protein Sci. 13, 1942-1947
16. Chan, K.-W., Lee, Y.-J., Wang, C.-H., Huang, H., and Sun, Y.-J. (2009) Single-stranded DNA-binding protein complex from Helicobacter pylori suggests an ssDNA-binding surface J. Mol. Biol. 388, 508-519
17. Kaushal, P. S., Singh, P., Sharma, A., Muniyappa, K., and Vijayan, M. (2010) X-ray and molecular-dynamics studies on Mycobacterium leprae single-stranded DNA-binding protein and comparison with other eubacterial SSB structures Acta Crystallogr. D66, 1048-1058
18. Antony, E., Weiland, E. A., Korolev, S., and Lohman, T. M. (2012) Plasmodium falciparum SSB tetramer wraps single-stranded DNA with similar topology but opposite polarity to E. coli SSB J. Mol. Biol. 420, 269-283
19. Yadav, T., Carrasco, B., Myers, A. R., George, N. P., Keck, J. L., and Alonso, J. C. (2012) Genetic recombination in Bacillus subtilis: A division of labor between two single-strand DNA-binding proteins Nucleic Acids Res. 40, 5546-5559
20. Cheng, Z., Caillet, A., Ren, B., and Ding, H. (2012) Stimulation of Escherichia coli DNA damage inducible DNA helicase DinG by the single-stranded DNA binding protein SSB FEBS Lett. 586, 3825-3830
21. Lu, D. and Keck, J. L. (2008) Structural basis of Escherichia coli single-stranded DNA-binding protein stimulation of exonuclease I Proc. Natl. Acad. Sci. U.S.A. 105, 9169-9174
22. Curth, U., Genschel, J., Urbanke, C., and Greipel, J. (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
23. Kozlov, A. G., Cox, M. M., and Lohman, T. M. (2010) Regulation of single-stranded DNA binding by the C termini of Escherichia coli single-stranded DNA-binding (SSB) protein J. Biol. Chem. 285, 17246-17252
24. Marintcheva, B., Marintchev, A., Wagner, G., and Richardson, C. C. (2008) Acidic C-terminal tail of the ssDNA-binding protein of bacteriophage T7 and ssDNA compete for the same binding surface Proc. Natl. Acad. Sci. U.S.A. 105, 1855-1860
25. Antony, E., Weiland, E., Yuan, Q., Manhart, C. M., Nguyen, B., Kozlov, A. G., McHenry, C. S., and Lohman, T. M. (2013) Multiple C-terminal tails within a single E. coli SSB homotetramer coordinate DNA replication and repair J. Mol. Biol. 425, 4802-4819
26. Shishmarev, D., Wang, Y., Mason, C. E., Su, X.-C., Oakley, A. J., Graham, B., Huber, T., Dixon, N. E., and Otting, G. (2014) Intramolecular binding mode of the C-terminus of E. coli single-stranded DNA binding protein (SSB) determined by nuclear magnetic resonance spectroscopy Nucleic Acids Res. 42, 2750-2757
27. 3+-spin labeling J. Am. Chem. Soc. 132, 9040-9048
28. 15N NMR relaxation Biochemistry 33, 5984-6003
29. Goddard, T. D. and Kneller, D. G. (2010) Sparky 3, University of California, San Francisco.
30. Record, M. T., Jr., Anderson, C. F., Mills, P., Mossing, M., and Roe, J. (1985) Ions as regulators of protein-nucleic acid interactions in vitro and in vivo Adv. Biophys. 20, 109-135
31. 13C]methionine UvrB from Bacillus caldotenax reveals UvrB-domain 4 heterodimer formation in solution J. Mol. Biol. 373, 282-295
32. 15N-relaxation J. Biomol. NMR 38, 65-72
33. García de la Torre, J., Huertas, M. L., and Carrasco, B. (2000) HYDRONMR: Prediction of NMR relaxation of globular proteins from atomic-level structures and hydrodynamic calculations J. Magn. Reson. 147, 138-146
34. Kontaxis, G., Clore, G. M., and Bax, A. (2000) Cross-correlation effects and measurements of one-bond couplings in proteins with short transverse relaxation times J. Magn. Reson. 143, 184-196
35. Witte, G., Urbanke, C., and Curth, U. (2003) DNA polymerase III - subunit ties single-stranded DNA binding protein to the bacterial replication machinery Nucleic Acids Res. 31, 4434-4440
36. Roy, R., Kozlov, A. G., Lohman, T. M., and Ha, T. (2007) Dynamic structural rearrangements between DNA binding modes of E. coli SSB protein J. Mol. Biol. 369, 1244-1257
37. Kozlov, A. G., Jezewska, M. J., Bujalowski, W., and Lohman, T. M. (2010) Binding specificity of Escherichia coli single-stranded DNA binding protein for the - subunit of DNA pol III holoenzyme and PriA helicase Biochemistry 49, 3555-3566
38. Griffith, J. D., Harris, L. D., and Register, J., III (1984) Visualization of SSB-ssDNA complexes active in the assembly of stable RecA-DNA filaments Cold Spring Harbor Symp. Quant. Biol. 49, 553-559
39. George, N. P., Ngo, K. V., Chitteni-Pattu, S., Norais, C. A., Battista, J. R., Cox, M. M., and Keck, J. L. (2012) Structure and cellular dynamics of Deinococcus radiodurans single-stranded DNA (ssDNA)-binding protein (SSB)-DNA complexes J. Biol. Chem. 287, 22123-22132
40. Chrysogelos, S. and Griffith, J. (1982) Escherichia coli single-strand binding protein organizes single-stranded DNA in nucleosome-like units Proc. Natl. Acad. Sci. U.S.A. 79, 5803-5807