A bacterial antirepressor with SH3 domain topology mimics operator DNA in sequestering the repressor DNA recognition helix

Nucleic Acids Research

Volumn 38, Issue 15, 2010, Pages 5226-5241

  León, Esther ^a   Navarro Avilés, Gloria ^b   Santiveri, Clara M ^a   Flores Flores, Cesar ^b   Rico, Manuel ^a   González, Carlos ^a   Murillo, Francisco J ^b   Elías Arnanz, Montserrat ^b   Jiménez, María Angeles ^a   Padmanabhan, S ^a  

^a INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^b CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARA PROTEIN; CARB PROTEIN; CARH PROTEIN; CARS PROTEIN; PROTEIN SH3; UNCLASSIFIED DRUG; CARS PROTEIN, MYXOCOCCUS XANTHUS; DNA; DNA BINDING PROTEIN; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; BETA SHEET; CONTROLLED STUDY; MOLECULAR RECOGNITION; MYXOCOCCUS XANTHUS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION INITIATION; AMINO ACID SEQUENCE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; MOLECULAR GENETICS; OPERATOR GENE; PROTEIN SECONDARY STRUCTURE; SRC HOMOLOGY DOMAIN;

BACTERIA (MICROORGANISMS); EUKARYOTA; MYXOCOCCUS XANTHUS; PROKARYOTA;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; DNA; DNA-BINDING PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OPERATOR REGIONS, GENETIC; PROTEIN STRUCTURE, SECONDARY; REPRESSOR PROTEINS; SRC HOMOLOGY DOMAINS; TRANSCRIPTION FACTORS;

EID: 77955165215     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq277     Document Type: Article

References (60)

1. Browning, D.F. and Busby, S.J. (2004) The regulation of bacterial transcription initiation. Nat. Rev. Microbiol., 2, 57-65.
2. Rojo,F. (2001) Mechanisms of transcriptional repression. Curr. Opin. Microbiol., 4, 145-151.
3. Schlax,P.J., Capp,M.W. and Record,M.T. Jr (1995) Inhibition of transcription initiation by lac repressor. J. Mol. Biol., 245, 331-350.
4. Oppenheim,A.B., Neubauer,Z. and Calef,E. (1970) The antirepressor: a new element in the regulation of protein synthesis. Nature, 226, 31-32.
5. Lewis,R.J., Brannigan,J.A., Offen,W.A., Smith,I. and Wilkinson,A.J. (1998) An evolutionary link between sporulation and prophage induction in the structure of a repressor:anti-repressor complex. J. Mol. Biol., 283, 907-912.
6. Luo,Y., Pfuetzner,R.A., Mosimann,S., Paetzel,M., Frey,E.A., Cherney,M., Kim,B., Little,J.W. and Strynadka,N.C.J. (2001) Crystal structure of LexA: a conformational switch for regulation of self-cleavage. Cell, 106, 585-594.
7. Davis,B.M., Kimsey,H.H., Kane,A.V. and Waldor,M.K. (2002) A satellite phage-encoded antirepressor induces repressor aggregation and cholera toxin gene transfer. EMBO J., 21, 4240-4249.
8. Masuda,S. and Bauer,C.E. (2002) AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell, 110, 613-623.
9. Wilke,M.S., Heller,M., Creagh,A.L., Haynes,C.A., McIntosh,L.P., Poole,K. and Strynadka,N.C. (2008) The crystal structure of MexR from Pseudomonas aeruginosa in complex with its ArmR. Proc. Natl Acad. Sci. USA, 105, 14832-14837.
10. Navarro-Avilés,G., Jiménez,M.A., Pérez-Marín,M.C., González,C., Rico,M., Murillo,F.J., Elías-Arnanz,M. and Padmanabhan,S. (2007) Structural basis for operator and antirepressor recognition by Myxococcus xanthus CarA repressor. Mol. Microbiol., 63, 980-994.
11. Elías-Arnanz,M., Fontes,M. and Padmanabhan,S. (2008) Carotenogenesis in Myxococcus xanthus: a complex regulatory network. Whitworth,D.E. (ed.), Myxobacteria: Multicellularity and Differentiation. ASM Press, Washington, DC, pp. 211-225.
12. López-Rubio,J.J., Elías-Arnanz,M., Padmanabhan,S. and Murillo,F.J. (2002) A repressor-antirepressor pair links two loci controlling light-induced carotenogenesis in Myxococcus xanthus. J. Biol. Chem., 277, 7262-7270.
13. Whitworth,D.E. and Hodgson,D.A. (2001) Light-induced carotenogenesis in Myxococcus xanthus: evidence that CarS acts as an anti-repressor of CarA. Mol. Microbiol., 42, 809-819.
14. López-Rubio,J.J., Padmanabhan,S., Lázaro,J.M., Salas,M., Murillo,F.J. and Elías-Arnanz,M. (2004) Operator design and mechanism for CarA repressor-mediated downregulation of the photo-inducible carB operon in Myxococcus xanthus. J. Biol. Chem., 279, 28945-28953.
15. 12 partners the CarH repressor to downregulate a photoinducible promoter in Myxococcus xanthus. Mol. Microbiol., 67, 804-819.
16. Kuriyan,J. and Cowburn,D. (1997) Modular peptide recognition domains in eukaryotic signaling. Annu. Rev. Biophys. Biomol. Struct., 26, 259-288.
17. D'Aquino,J.A. and Ringe,D. (2003) Determinants of the Src homology domain 3-like fold. J. Bacteriol., 185, 4081-40.
18. Li,S.S. (2005) Specificity and versatility of SH3 and other proline-recognition domains: structural basis and implications for cellular signal transduction. Biochem. J., 390, 641-653.
19. Ho,S.N., Hunt,H.D., Horton,R.M., Pullen,J.K. and Pease,L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene, 77, 51-59.
20. León,E., González,C., Elías-Arnanz,M., Padmanabhan,S. and Jiménez,M.A. (2009) 1H, 13C and 15N backbone and side chain resonance assignments of a Myxococcus xanthus antirepressor with no known sequence homologues. Biomol. NMR Assign., 3, 37-40.
21. Guntert,P. (2004) Automated NMR structure calculation with CYANA. Methods Mol. Biol., 278, 353-378.
22. Cornilescu,G., Delaglio,F. and Bax,A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR, 13, 289-302.
23. Case,D.A., Perlman,D.A., Caldwell,J.W., Cheatham III,T.E., Wang,J., Ross,W.S., Simmerling,C., Darden,T., Merz,K.M., Stanton,R.V. et al. (2002) AMBER 7. University of California, San Francisco.
24. Laskowski,R.A., Rullmannn,J.A., MacArthur,M.W., Kaptein,R. and Thornton,J.M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR, 8, 477-486.
25. Willard,L., Ranjan,A., Zhang,H., Monzavi,H., Boyko,R.F., Sykes,B.D. and Wishart,D.S. (2003) VADAR: a web server for quantitative evaluation of protein structure quality. Nucleic Acids Res., 31, 3316-3319.
26. Koradi,R., Billeter,M. and Wüthrich,K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph., 14, 51-58.
27. Bai,Y., Milne,J.S., Mayne,L. and Englander,S.W. (1994) Protein stability parameters measured by hydrogen exchange. Proteins, 20, 4-14.
28. Morris,G.A. and Freeman,R. (1979) Enhancement of nuclear magnetic resonance signals by polarization transfer. J. Am. Chem. Soc., 101, 760-762.
29. Grzesiek,S., Stahl,S.J., Wingfield,P.T. and Bax,A. (1996) The CD4 determinant for down-regulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR. Biochemistry, 35, 10256-10261.
30. Peñalver-Mellado,M., García-Heras,F., Padmanabhan,S., García-Moreno,D., Murillo,F.J. and Elías-Arnanz,M. (2006) Recruitment of a novel zinc-bound transcriptional factor by a bacterial HMGA-type protein is required for regulating multiple processes in Myxococcus xanthus. Mol. Microbiol., 61, 910-926.
31. Dominguez,C., Boelens,R. and Bonvin,A.M. (2003) HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J. Am. Chem. Soc., 125, 1731-1737.
32. Soliva,R., Monaco,V., Gómez-Pinto,I., Meeuwenoord,N.J., Marel,G.A., Boom,J.H., González,C. and Orozco,M. (2001) Solution structure of a DNA duplex with a chiral alkyl phosphonate moiety. Nucleic Acids Res, 29, 2973-2985.
33. Cornell,W.D., Cieplak,P., Bayly,C.I., Gould,I.R., Merz,K., Ferguson,D.M., Spellmeyer,D.C., Fox,T., Caldwell,J.W. and Kollman,P.A. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc., 117, 5179-5197.
34. Jorgensen,W.L., Chandrasekhar,J., Madura,J.D., Impey,R.W. and Klein,M.L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys., 79, 926-935.
35. Darden,T.E., York,D. and Pedersen,L. (1993) Particle mesh Ewald: An N·log(N) method for Ewald sums in large systems. J. Chem. Phys., 98, 10089-10092.
36. Pérez-Marín,M.C., López-Rubio,J.J., Murillo,F.J., Elías-Arnanz,M. and Padmanabhan,S. (2004) The N-terminus of M. xanthus CarA repressor is an autonomously folding domain that mediates physical and functional interactions with both operator DNA and antirepressor protein. J. Biol. Chem., 279, 33093-33103.
37. Holm,L. and Sander,C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol., 233, 23-38.
38. Narayana,N., Matthews,D.A., Howell,E.E. and Nguyen-huu,X. (1995) A plasmid-encoded dihydrofolate reductase from trimethoprim-resistant bacteria has a novel D2-symmetric active site. Nat. Struct. Biol., 2, 1018-1025.
39. Dai,S., Schwendtmayer,C., Schürmann,P., Ramaswamy,S. and Eklund,H. (2000) Redox signaling in chloroplasts: cleavage of disulfides by an iron-sulfur cluster. Science, 287, 655-658.
40. Padmanabhan,S., Marqusee,S., Ridgeway,T., Laue,T.M. and Baldwin,R.L. (1989) Relative helix-forming tendencies of nonpolar amino acids. Nature, 344, 268-270.
41. Padmanabhan,S., Zhang,W., Capp,M.W., Anderson,C.F. and Record,M.T. Jr (1997) Binding of cationic (+4) alanine- and glycine-containing oligopeptides to double-stranded DNA: thermodynamic analysis of effects of coulombic interactions and alpha-helix induction. Biochemistry, 36, 5193-5206.
42. Spolar,R.S. and Record,M.T. Jr (1994) Coupling of local folding to site-specific binding of proteins to DNA. Science, 263, 777-784.
43. Demers,J.P. and Mittermaier,A. (2009) Binding mechanism of an SH3 domain studied by NMR and ITC. J. Am. Chem. Soc., 131, 4355-4367.
44. Douangamath,A., Filipp,F.V., Klein,A.T., Barnett,P., Zou,P., Voorn-Brouwer,T., Vega,M.C., Mayans,O.M., Sattler,M., Distel,B. et al. (2002) Topography for independent binding of alpha-helical and PPII-helical ligands to a peroxisomal SH3 domain. Mol. Cell, 10, 1007-1017.
45. Kami,K., Takeya,R., Sumimoto,H. and Kohda,D. (2002) Diverse recognition of non-PxxP peptide ligands by the SH3 domains from p67(phox), Grb2 and Pex13p. EMBO J., 21, 4268-4276.
46. Stamenova,S.D., French,M.E., He,Y., Francis,S.A., Kramer,Z.B. and Hicke,L. (2007) Ubiquitin binds to and regulates a subset of SH3 domains. Mol. Cell, 25, 273-284.
47. Trempe,J.-F., Chen,C.X.-Q., Grenier,K., Camacho,E.M., Kozlov,G., McPherson,P.S., Gehring,K. and Fon,E.A. (2009) SH3 domains from a subset of BAR proteins define a Ubl-binding domain and implicate parkin in synaptic ubiquitination. Mol. Cell, 36, 1034-1047.
48. Delbrück,H., Ziegelin,G., Lanka,E. and Heinemann,U. (2002) An Src homology 3-like domain is responsible for dimerization of the repressor protein KorB encoded by the promiscuous IncP plasmid RP4. J. Biol. Chem., 277, 4191-4198.
49. Wang,G., Wylie,G.P., Twigg,P.D., Caspar,D.L., Murphy,J.R. and Logan,T.M. (1999) Solution structure and peptide binding studies of the C-terminal src homology 3-like domain of the diphtheria toxin repressor protein. Proc. Natl Acad. Sci. USA, 96, 6119-6124.
50. Hodgson,D.A. (1993) Light-induced carotenogenesis in Myxococcus xanthus: genetic analysis of the carR region. Mol. Microbiol., 7, 471-488.
51. Putnam,C.D. and Tainer,J.A. (2005) Protein mimicry of DNA and pathway regulation. DNA Repair, 4, 1410-1420.
52. Dryden,D.T.F. (2006) DNA mimicry by proteins and the control of enzymatic activity on DNA. Trends Biotechnol., 4, 378-382.
53. Walkinshaw,M.D., Taylor,P., Sturrock,S.S., Atanasiu,C., Berge,T., Henderson,R.M., Edwardson,J.M. and Dryden,D.T.F. (2002) Structure of Ocr from bacteriophage T7, a protein that mimics B-form DNA. Mol. Cell, 9, 187-194.
54. McMahon,S.A., Roberts,G.A., Johnson,K.A., Cooper,L.P., Liu,H., White,J.H., Carter,L.G., Sanghvi,B., Oke,M., Walkinshaw,M.D. et al. (2009) Extensive DNA mimicry by the ArdA anti-restriction protein and its role in the spread of antibiotic resistance. Nucleic Acids Res., 37, 4887-4897.
55. Mol,C.D., Arvai,A.S., Sanderson,R.J., Slupphaug,G., Kavli,B., Krokan,H.E., Mosbaugh,D.W. and Tainer,J.A. (1995) Crystal structure of human uracil-DNA glycosylase in complex with a protein inhibitor: protein mimicry of DNA. Cell, 82, 701-708.
56. Serrano-Heras,G., Ruiz-Masó,J.A., del Solar,G., Espinosa,M., Bravo,A. and Salas,M. (2007) Protein p56 from the Bacillus subtilis phage ø29 inhibits DNA-binding ability of uracil-DNA glycosylase. Nucleic Acids Res., 35, 5393-5401.
57. Hegde,S.S., Vetting,M.W., Roderick,S.L., Mitchenall,L.A., Maxwell,A., Takiff,H.E. and Blanchard,J.S. (2005) A fluoroquinolone resistance protein from Mycobacterium tuberculosis that mimics DNA. Science, 308, 1480-1483.
58. Parsons,L.M., Liu,F. and Orban,J. (2005) HU-alpha binds to the putative double-stranded DNA mimic HI1450 from Haemophilus influenzae. Protein Sci., 14, 1684-1687.
59. Wang,H.C., Wang,H.C., Ko,T.P., Lee,Y.M., Leu,J.H., Ho,C.H., Huang,W.P., Lo,C.F. and Wang,A.H. (2008) White spot syndrome virus protein ICP11: A histone-binding DNA mimic that disrupts nucleosome assembly. Proc. Natl Acad. Sci. USA, 105, 20758-20763.
60. ||230 complex: protein mimicry of the minor groove surface of the TATA box unwound by TBP. Cell, 94, 573-583.