Single-stranded DNA binding of the cold-shock protein CspB from Bacillus subtilis: NMR mapping and mutational characterization

Protein Science

Volumn 12, Issue 1, 2003, Pages 112-123

  Zeeb, Markus ^a   Balbach, Jochen ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

Cold shock protein; CspB; NMR spectroscopy; Protein ssDNA complex; Single stranded DNA; Y Box

Indexed keywords

AROMATIC AMINO ACID; COLD SHOCK PROTEIN; PHENYLALANINE; RIBONUCLEOPROTEIN; RNA; SINGLE STRANDED DNA;

AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS SUBTILIS; BINDING AFFINITY; CONFORMATION; DNA BINDING; FLUORESCENCE; GENE MAPPING; KINETICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN VARIANT; PROTON NUCLEAR MAGNETIC RESONANCE; RNA BINDING; TITRIMETRY;

AMINO ACID SUBSTITUTION; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BINDING SITES; CONSERVED SEQUENCE; DNA, SINGLE-STRANDED; KINETICS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE MAPPING; PHENYLALANINE; PROTEIN BINDING; PROTEIN CONFORMATION; RNA-BINDING PROTEINS; SPECTROMETRY, FLUORESCENCE; THERMODYNAMICS; TRYPTOPHAN;

BACILLUS SUBTILIS; POSIBACTERIA;

EID: 0037216364     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.0219703     Document Type: Article

References (68)

1. Berg, O.G., Winter, R.B., and von Hippel, P.H. 1981. Diffusion-driven mechanisms of protein translocation on nucleic acids. 1. Models and theory. Biochemistry 20: 6929-6948.
2. Bernasconi, C.F. 1976. Relaxation Kinetics. Academic Press, New York.
3. Billeter, M., Qian, Y.Q., Otting, G., Müller, M., Gehring, W., and Wüthrich, K. 1993. Determination of the nuclear magnetic resonance solution structure of an Antennapedia homeodomain-DNA complex. J. Mol. Biol. 234: 1084-1093.
4. Brandi, A., Pietroni, P., Gualerzi, C.O., and Pon, C.L. 1996. Post-transcriptional regulation of CspA expression in Escherichia coli. Mol. Microbiol. 19: 231-240.
5. Brandi, A., Spurio, R., Gualerzi, C.O., and Pon, C.L. 1999. Massive presence of the Escherichia coli "major cold-shock protein" CspA under non-stress conditions. EMBO J. 18: 1653-1659.
6. Cerdan, R., Payet, D., Yang, J.C., Travers, A.A., and Neuhaus, D. 2001. HMG-D complexed to a bulge DNA: An NMR model. Protein Sci. 10: 504-518.
7. Didier, D.K., Schiffenbauer, J., Woulfe. S.L., Zacheis, M., and Schwartz, B.D. 1988. Characterization of the cDNA encoding a protein binding to the major histocompatibility complex class II Y box. Proc. Natl. Acad. Sci. 85: 7322-7326.
8. Dong, F., Spott, S., Zimmermann, O., Kisters-Woike, B., Muller-Hill. B., and Barker, A. 1999. Dimerisation mutants of Lac repressor. I. A monomeric mutant, L251A, that binds Lac operator DNA as a dimer. J. Mol. Biol. 290: 653-666.
9. Draper, D.E. and Reynaldo, L.P. 1999. RNA binding strategies of ribosomal proteins. Nucleic Acid Res. 27: 381-388.
10. Eftink, M.R. 1997. Fluorescence methods for studying equilibrium macromolecule-ligand interactions. Methods Enzymol. 278: 221-257.
11. Feng, W., Tejero, R., Zimmerman, D.E., Inouye, M., and Montelione, G.T. 1998. Solution NMR structure and backbone dynamics of the major cold-shock protein (CspA) from Escherichia coli: Evidence for conformational dynamics in the single-stranded RNA-binding site. Biochemistry 37: 10881-10896.
12. Foster, M.P., Wuttke, D.S., Radhakrishnan, I., Case, D.A., Gottesfeld, J.M., and Wright, P.E. 1997. Domain packing and dynamics in the DNA complex of the N-terminal zinc fingers of TFIIIA. Nat. Struct. Biol. 4: 605-608.
13. Gill, S.C. and von Hippel, P.H. 1989. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182: 319-326.
14. Goldenberg, D., Azar, I., and Oppenheim, A.B. 1996. Differential mRNA stability of the cspA gene in the cold-shock response of Escherichia coli. Mol. Microbiol. 19: 241-248.
15. Gomis-Rüth, F.X., Sola, M., Acebo, P., Parraga, A., Guasch, A., Eritja, R., Gonzalez, A., Espinosa, M., del Solar, G., and Coll, M. 1998. The structure of plasmid-encoded transcriptional repressor CopG unliganded and bound to its operator. EMBO J. 17: 1704-1715.
16. Graumann, P. and Marahiel, M.A. 1994. The major cold shock protein of Bacillus subtilis CspB binds with high affinity to the ATTGG- and CCAAT sequences in single stranded oligonucleotides. FEBS Lett. 338: 157-160.
17. Graumann, P., Wendrich, T.M., Weber, M.H., Schröder, K., and Marahiel, M.A. 1997. A family of cold shock proteins in Bacillus subtilis is essential for cellular growth and for efficient protein synthesis at optimal and low temperatures. Mol. Microbiol. 25: 741-756.
18. Graumann, P.L. and Marahiel, M.A. 1998. A superfamily of proteins that contain the cold-shock domain. Trends Biochem. Sci. 23: 286-290.
19. Grzesiek, S., Stahl, S.J., Wingfield, P.T., and Bax, A. 1996. The CD4 determinant for downregulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR. Biochemistry 35: 10256-10261.
20. Hebraud, M. and Potier, P. 1999. Cold shock response and low temperature adaptation in psychrotrophic bacteria. J. Mol. Microbiol. Biotechnol. 1: 211-219.
21. Henkin, T.M. 1996. Control of transcription termination in prokaryotes. Annu. Rev. Genet. 30: 35-57.
22. Hingorani, M.M. and O'Donnell, M. 2000. Sliding clamps: A (tail)ored fit. Curr. Biol. 10: 25-29.
23. Hoopes, B.C., LeBlanc, J.F., and Hawley, D.K. 1998. Contributions of the TATA box sequence to rate-limiting steps in transcription initiation by RNA polymerase II. J. Mol. Biol. 277: 1015-1031.
24. Horvath, M.P., Schweiker, V.L., Bevilacqua, J.M., Ruggles, J.A., and Schultz, S.C. 1998. Crystal structure of the Oxytricha nova telomere end binding protein complexed with single strand DNA. Cell 95: 963-974.
25. Iwahara, J., Wojciak, J.M., and Clubb, R.T. 2001. Improved NMR spectra of a protein-DNA complex through rational mutagenesis and the application of a sensitivity optimized isotope-filtered NOESY experiment. J. Biomol. NMR. 19: 231-241.
26. Jiang, W., Jones, P., and Inouye, M. 1993. Chloramphenicol induces the transcription of the major cold shock gene of Escherichia coli, cspA. J. Bacteriol. 175: 5824-5828.
27. Jiang, W., Hou, Y., and Inouye, M. 1997. CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J. Biol. Chem. 272: 196-202.
28. Jones, P.G. and Inouye, M. 1994. The cold-shock response - A hot topic. Mol. Microbiol. 11: 811-818.
29. Jones, P.G., VanBogelen, R.A., and Neidhardt, F.C. 1987. Induction of proteins in response to low temperature in Escherichia coli. J. Bacteriol. 169: 2092-2095.
30. Jones, P.G., Krah, R., Tafuri, S.R., and Wolffe, A.P, 1992. DNA gyrase, CS7.4, and the cold shock response in Escherichia coli. J. Bacteriol. 174: 5798-5802.
31. Katsamba, P.S., Myszka, D.G., and Laird-Offringa, I.A. 2001. Two functionally distinct steps mediate high affinity binding of U1A protein to U1 hairpin II RNA. J. Biol. Chem. 276: 21476-21481.
32. Kay, L., Keifer, P., and Saarinen, T. 1992. Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved senitivity. J. Am. Chem. Soc. 114: 10663-10665.
33. Kloks, C.P., Spronk, C.A., Lasonder, E., Hoffmann, A., Vuister, G.W., Grzesiek, S., and Hilbers. C.W. 2002. The solution structure and DNA-binding properties of the cold-shock domain of the human Y-box protein YB-1. J. Mol. Biol. 316: 317-326.
34. Koradi, R., Billeter, M., and Wüthrich, K. 1996. MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graph. 14: 51-55.
35. Lohman, T.M. and Bujalowski, W. 1991. Thermodynamic methods for model-independent determination of equilibrium binding isotherms for protein-DNA interactions: Spectroscopic approaches to monitor binding. Methods Enzymol. 208: 258-290.
36. Lopez, M.M. and Makhatadze, G.I. 2000. Major cold shock proteins, CspA from Escherichia coli and CspB from Bacillus subtilis, interact differently with single-stranded DNA templates. Biochim. Biophys. Acta 1479: 196-202.
37. Lopez, M.M., Yutani, K., and Makhatadze. G.I. 1999. Interactions of the major cold shock protein of Bacillus subtilis CspB with single-stranded DNA templates of different base composition. J. Biol. Chem. 274: 33601-33608.
38. -, 2001. Interactions of the cold shock protein CspB from Bacillus subtilis with single-stranded DNA. Importance of the T base content and the position within the template. J. Biol. Chem. 276: 15511-15518.
39. Mayr, L.M., Landt, O., Hahn, U., and Schmid, F.X. 1993. Stability and folding kinetics of ribonuclease T1 are strongly altered by the replacement of cisproline 39 with alanine. J. Mol. Biol. 231: 897-912.
40. Meiering, E.M., Serrano, L., and Fersht, A.R. 1992. Effect of active site residues in barnase on activity and stability. J. Mol. Biol. 225: 585-589.
41. Murzin, A.G. 1993. OB (oligonucleotide/oligosaccharide binding)-fold: Common structural and functional solution for non-homologous sequences. EMBO J. 12: 861-867.
42. Nakagawa, A., Nakashima, T., Taniguchi, M., Hosaka, H., Kimura, M., and Tanaka, I. 1999. The three-dimensional structure of the RNA-binding domain of ribosomal protein L2; A protein at the peptidyl transferase center of the ribosome. EMBO J. 18: 1459-1467.
43. Newkirk, K., Feng, W., Jiang, W., Tejero, R., Emerson, S.D., Inouye, M., and Montelione, G.T. 1994. Solution NMR structure of the major cold shock protein (CspA) from Escherichia coli: Identification of a binding epitope for DNA. Proc. Natl. Acad. Sci, 91: 5114-5118.
44. Neylon, C., Brown, S.E., Kralicek, A.V., Miles, C.S., Love, C.A., and Dixon, N.E. 2000. Interaction of the Escherichia coli replication terminator protein (Tus) with DNA: A model derived from DNA-binding studies of mutant proteins by surface plasmon resonance. Biochemistry 39: 11989-11999.
45. Palmer III, A.G., Cavanagh, J., Wright, P.E., and Rance, M. 1991. Sensitivity improvement in proton-detected 2-dimensional heteronuclear correlation NMR-spectroscopy. J. Magn. Reson. 93: 151-170.
46. Pelletier, M., Miller, M.M., and Read, L.K. 2000. RNA-binding properties of the mitochondrial Y-box protein RBP16. Nucleic Acids Res. 28: 1266-1275.
47. Phadtare, S. and Inouye, M. 1999. Sequence-selective interactions with RNA by CspB, CspC and CspE, members of the CspA family of Escherichia coli. Mol. Microbiol. 33: 1004-1014.
48. Phadtare, S., Alsina, J., and Inouye, M. 1999. Cold-shock response and cold-shock proteins. Curr. Opin. Microbiol. 2: 175-180.
49. Phillips, R.J., Hickleton, D.C., Boehmer, P.E., and Emmerson, P.T. 1997. The RecB protein of Escherichia coli translocates along single-stranded DNA in the 3′ to 5′ direction: A proposed ratchet mechanism. Mol. Gen. Genet. 254: 319-329.
50. Piotto, M., Saudek, V., and Sklenar, V. 1992. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2: 661-665.
51. Richardson, J.P. 1993. Transcription termination. Crit. Rev. Biochem. Mol. Biol. 28: 1-30.
52. Sandström, J. 1982. Dynamic NMR Spectroscopy. Academic Press. New York.
53. Schindelin, H., Herrler, M., Willimsky, G., Marahiel, M.A., and Heinemann, U. 1992. Overproduction, crystallization, and preliminary X-ray diffraction studies of the major cold shock protein from Bacillus subtilis, CspB. Proteins 14: 120-124.
54. Schindelin, H., Marahiel, M.A., and Heinemann, U. 1993. Universal nucleic acid-binding domain revealed by crystal structure of the B. subtilis major cold-shock protein. Nature 364: 164-168.
55. Schindelin, H., Jiang, W., Inouye, M., and Heinemann, U. 1994. Crystal structure of CspA, the major cold shock protein of Escherichia coli. Proc. Natl. Acad. Sci. 91: 5119-5123.
56. Schindler, T., Herrler, M., Marahiel, M.A., and Schmid, F.X. 1995. Extremely rapid folding in the absence of intermediates: The cold-shock protein from Bacillus subtilis. Nat. Struct. Biol. 2: 663-673.
57. Schindler, T., Perl, D., Graumann, P., Sieber, V., Marahiel, M.A., and Schmid, F.X. 1998. Surface-exposed phenylalanines in the RNP1/RNP2 motif stabilize the cold-shock protein CspB from Bacillus subtilis. Proteins 30: 401-406.
58. Schindler, T., Graumann, P.L., Perl, D., Ma, S., Schmid, F.X., and Marahiel, M.A. 1999. The family of cold shock proteins of Bacillus subtilis. Stability and dynamics in vitro and in vivo. J. Biol. Chem. 274: 3407-3413.
59. Schleucher, J., Schwendinger, M., Sattler, M., Schmidt, P., Schedletzky, O., Glaser, S.J., Sørensen, O.W., and Griesinger, C. 1994. A general enhancement scheme in heteronuclear multidimensional NMR employing pulsedfield gradients. J. Biomol. NMR 4: 301-306.
60. Schnuchel, A., Wiltschek, R., Czisch, M., Herrler, M., Willimsky, G., Graumann, P., Marahiel, M.A., and Holak, T.A. 1993. Structure in solution of the major cold-shock protein from Bacillus subtilis. Nature 364: 169-171.
61. Schreiber, C., Buckle, A.M., and Fersht, A.R. 1994. Stability and function: Two constraints in the evolution of barstar and other proteins. Structure 2: 945-951.
62. Schröder, K., Graumann, P., Schnuchel, A., Holak, T.A., and Marahiel, M.A. 1995. Mutational analysis of the putative nucleic acid-binding surface of the cold-shock domain, CspB, revealed an essential role of aromatic and basic residues in binding of single-stranded DNA containing the Y-box motif. Mol. Microbiol. 16: 699-708.
63. Sette, M., van Tilborg, P., Spurio, R., Kaptein, R., Paci, M., Gualerzi, C.O., and Boelens, R. 1997. The structure of the translational initiation factor IFI from E. coli contains an oligomer-binding motif. EMBO J. 16: 1436-1443.
64. Shoichet, B.K., Baase, W.A., Kuroki, R., and Matthews, B.W. 1995. A relationship between protein stability and protein function. Proc. Natl. Acad. Sci. 92: 452-456.
65. Tonomura, B., Nakatani, H., Ohnishi, M., Yamaguchi-Ito, J., and Hiromi, K. 1978. Test reaction for a stopped-flow apparatus. Anal. Biochem. 84: 370-383.
66. Wallace, R.B., and Miyada, C.G. 1987. Oligonucleotide probes for the screening of recombinant DNA libraries. Methods Enzymol. 152: 432-442.
67. Werten, S., Wechselberger, R., Boelens, R., van der Vliet, P.C., and Kaptein, R. 1999. Identification of the single-stranded DNA binding surface of the transcriptional coactivator PC4 by NMR. J. Biol. Chem. 274: 3693-3699.
68. Yamanaka, K., Fang, L., and Inouye, M. 1998. The CspA family in Escherichia coli: Multiple gene duplication for stress adaptation. Mol. Microbiol. 27: 247-255.