Interaction investigations of HipA binding to HipB dimer and HipB dimer + DNA complex: A molecular dynamics simulation study

Journal of Molecular Recognition

Volumn 26, Issue 11, 2013, Pages 556-567

  Li, Chaoqun ^a   Wang, Yaru ^a   Wang, Yan ^a   Chen, Guangju ^a  

^a BEIJING NORMAL UNIVERSITY   (China)

Author keywords

allosteric communication; binding free energy; HipA HipB DNA; MD simulation; mechanism of sequestration

Indexed keywords

DNA; DNA BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; HIPA PROTEIN, E COLI; HIPB PROTEIN, E COLI;

ALLOSTERIC COMMUNICATION; ARTICLE; BINDING FREE ENERGY; CHEMISTRY; CONFORMATION; ESCHERICHIA COLI; HIPA/HIPB/DNA; HYDROGEN BOND; MD SIMULATION; MECHANISM OF SEQUESTRATION; METABOLISM; MOLECULAR DYNAMICS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; STATIC ELECTRICITY; THERMODYNAMICS; TIME;

ALLOSTERIC COMMUNICATION; BINDING FREE ENERGY; HIPA/HIPB/DNA; MD SIMULATION; MECHANISM OF SEQUESTRATION;

DNA; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROGEN BONDING; MOLECULAR DYNAMICS SIMULATION; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; STATIC ELECTRICITY; THERMODYNAMICS; TIME FACTORS;

EID: 84885593195     PISSN: 09523499     EISSN: 10991352     Source Type: Journal    
DOI: 10.1002/jmr.2300     Document Type: Article

References (61)

1. Alexander C, Bilgin N, Lindschau C, Mesters JR, Kraal B, Hilgenfeld R, Erdmann VA, Lippmann C,. 1995. Phosphorylation of elongation factor Tu prevents ternary complex formation. J. Biol. Chem. 270: 14541- 14547.
2. Archambaud C, Gouin E, Pizarro-Cerda J, Cossart P, Dussurget O,. 2005. Translation elongation factor EF-Tu is a target for Stp, a serine-threonine phosphatase involved in virulence of Listeria monocytogenes. Mol. Microbiol. 56: 383-396.
3. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S,. 2004. Bacterial persistence as a phenotypic switch. Science 305: 1622-1625.
4. Basdevant N, Weinstein H, Ceruso M,. 2006. Thermodynamic basis for promiscuity and selectivity in protein-protein interactions: PDZ domains, a case study. J. Am. Chem. Soc. 128: 12766- 12777.
5. Bigger J,. 1944. Treatment of staphylococcal infections with penicillin by intermittent sterilisation. Lancet 244: 497-500.
6. Billeter M, Qian YQ, Otting G, Müller M, Gehring W, Wüthrich K,. 1993. Determination of the nuclear magnetic resonance solution structure of an antennapedia homeodomain-DNA complex. J. Mol. Biol. 234: 1084-1097.
7. Black DS, Irwin B, Moyed HS,. 1994. Autoregulation of hip, an operon that affects lethality due to inhibition of peptidoglycan or DNA synthesis. J. Bacteriol. 176: 4081-4091.
8. Black DS, Kelly AJ, Mardis M, Moyed HS,. 1991. Structure and organization of hip, an operon that affects lethality due to inhibition of peptidoglycan or DNA synthesis. J. Bacteriol. 173: 5732-5739.
9. Blakaj DM, McConnell KJ, Beveridge DL, Baranger AM,. 2001. Molecular dynamics and thermodynamics of protein-RNA interactions: mutation of a conserved aromatic residue modifies stacking interactions and structural adaptation in the U1A-stem loop 2 RNA complex. J. Am. Chem. Soc. 123: 2548-2551.
10. Brocklehurst SM, Perham RN,. 1993. Prediction of the three-dimensional structures of the biotinylated domain from yeast pyruvate carboxylase and of the lipoylated H-protein from the pea leaf glycine cleavage system: a new automated method for the prediction of protein tertiary structure. Protein Sci. 2: 626-639.
11. Brooun A, Liu S, Lewis K,. 2000. A dose-response study of antibiotic resistance in pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 44: 640-646.
12. Buts L, Lah J, Dao-Thi MH, Wyns L, Loris R,. 2005. Toxin-antitoxin modules as bacterial metabolic stress managers. Trends Biochem. Sci. 30: 672-679.
13. Case DA, Darden T, Cheatham III TE, Simmerling C, Wang J, Duke RE, Luo R, Merz KM, Pearlman DA, Crowley M, Walker R, Zhang W, Wang B, Hayik S, Roitberg A, Seabra G, Wong K, Paesani F, Wu X, Brozell S, Tsui V, Gohlke H, Yang L, Tan C, Mongan J, Hornak V, Cui G, Beroza P, Mathews DH, Schafmeister C, Ross WS, Kollman PA,. 2006. AMBER 9. University of California: San Francisco.
14. Cheatham III TE, Srinivasan J, Case DA, Kollman PA,. 1998. Molecular dynamics and continuum solvent studies of the stability of polyG-polyC and polyA-polyT DNA duplexes in solution. J. Biomol. Struct. Dyn. 16: 265-280.
15. Chen L, Zhang JL, Yu LY, Zheng QC, Chu WT, Xue Q, Zhang HX, Sun CC,. 2012. Influence of hyperthermophilic protein Cren7 on the stability and conformation of DNA: insights from molecular dynamics simulation and free energy analysis. J. Phys. Chem. B 116: 12415- 12425.
16. Chuprina V, Rullmann J, Lamerichs R, Van Boom J, Boelens R, Kaptein R,. 1993. Structure of the complex of lac repressor headpiece and an 11 base-pair half-operator determined by nuclear magnetic resonance spectroscopy and restrained molecular dynamics. J. Mol. Biol. 234: 446.
17. Correia FF, D'Onofrio A, Rejtar T, Li L, Karger BL, Makarova K, Koonin EV, Lewis K,. 2006. Kinase activity of overexpressed HipA is required for growth arrest and multidrug tolerance in Escherichia coli. J. Bacteriol. 188: 8360-8367.
18. Duan Y, Wu C, Chowdhury S, Lee MC, Xiong G, Zhang W, Yang R, Cieplak P, Luo R, Lee T,. 2003. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J. Comput. Chem. 24: 1999- 2012.
19. Evdokimov A, Voznesensky I, Fennell K, Anderson M, Smith JF, Fisher DA,. 2009. New kinase regulation mechanism found in HipBA: a bacterial persistence switch. Acta Crystallogr. D Biol. Crystallogr. 65: 875-879.
20. Falla T, Chopra I,. 1999. Stabilization of Rhizobium symbiosis plasmids. Microbiology 145: 515-516.
21. Falla TJ, Chopra I,. 1998. Joint tolerance to β-lactam and fluoroquinolone antibiotics in Escherichia coli results from overexpression of hipA. Antimicrob. Agents Chemother. 42: 3282-3284.
22. Gerdes K, Christensen SK, Lobner-Olesen A,. 2005. Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 3: 371-382.
23. Gohlke H, Case DA,. 2004. Converging free energy estimates: MM-PB (GB) SA studies on the protein-protein complex Ras-Raf. J. Comput. Chem. 25: 238-250.
24. Grünberg R, Nilges M, Leckner J,. 2006. Flexibility and conformational entropy in protein-protein binding. Structure 14: 683-693.
25. Hansen S, Lewis K, Vulic̈ M,. 2008. Role of global regulators and nucleotide metabolism in antibiotic tolerance in Escherichia coli. Antimicrob. Agents Chemother. 52: 2718-2726.
26. Hansen S, Vulic M, Min J, Yen TJ, Schumacher MA, Brennan RG, Lewis K,. 2012. Regulation of the Escherichia coli HipBA toxin-antitoxin system by proteolysis. PloS One 7: e39185.
27. Hou T, Wang J, Li Y, Wang W,. 2010. Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations. J. Chem. Inf. Model. 51: 69-82.
28. Jayaram B, Sprous D, Young M, Beveridge D,. 1998. Free energy analysis of the conformational preferences of A and B forms of DNA in solution. J. Am. Chem. Soc. 120: 10629- 10633.
29. Jayaraman R,. 2008. Bacterial persistence: some new insights into an old phenomenon. J. Biosci. 33: 795-805.
30. Jensen F,. 2007. Introduction to computational chemistry. Wiley: West Sussex.
31. Keren I, Kaldalu N, Spoering A, Wang Y, Lewis K,. 2004a. Persister cells and tolerance to antimicrobials. FEMS Microbiol. Lett. 230: 13-18.
32. Keren I, Shah D, Spoering A, Kaldalu N, Lewis K,. 2004b. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J. Bacteriol. 186: 8172-8180.
33. Kollman PA, Massova I, Reyes C, Kuhn B, Huo S, Chong L, Lee M, Lee T, Duan Y, Wang W,. 2000. Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Acc. Chem. Res. 33: 889-897.
34. Korch SB, Henderson TA, Hill TM,. 2003. Characterization of the hipA7 allele of Escherichia coli and evidence that high persistence is governed by (p) ppGpp synthesis. Mol. Microbiol. 50: 1199-1213.
35. Kormos BL, Benitex Y, Baranger AM, Beveridge DL,. 2007. Affinity and specificity of protein U1A-RNA complex formation based on an additive component free energy model. J. Mol. Biol. 371: 1405-1419.
36. Kottalam J, Case D,. 2004. Langevin modes of macromolecules: applications to crambin and DNA hexamers. Biopolymers 29: 1409-1421.
37. Kuhn B, Kollman PA,. 2000. Binding of a diverse set of ligands to avidin and streptavidin: an accurate quantitative prediction of their relative affinities by a combination of molecular mechanics and continuum solvent models. J. Med. Chem. 43: 3786-3791.
38. Lavery R, Sklenar H,. 1988. The definition of generalized helicoidal parameters and of axis curvature for irregular nucleic acids. J. Biomol. Struct. Dyn. 6: 63-91.
39. Lavery R, Sklenar H,. 1996. Curves 5.2: helical analysis of irregular nucleic acids; Laboratoire de Biochimie Theorique. CNRS URA 77: 1-29.
40. Lee MC, Duan Y,. 2004. Distinguish protein decoys by using a scoring function based on a new AMBER force field, short molecular dynamics simulations, and the generalized born solvent model. Proteins 55: 620-634.
41. Lewis K,. 2007. Persister cells, dormancy and infectious disease. Nature Rev. Microbiol. 5: 48-56.
42. Lewis K,. 2008. Multidrug tolerance of biofilms and persister cells. Curr. Top. Microbiol. Immunol. 322: 107-131.
43. Lewis K, Hansen S,. 2013. Type II toxin-antitoxin loci, hipBA and persisters. In Prokaryotic toxin-antitoxins. Springer: New York, 189-203.
44. Lippmann C, Lindschau C, Vijgenboom E, Schröder W, Bosch L, Erdmann V,. 1993. Prokaryotic elongation factor Tu is phosphorylated in vivo. J. Biol. Chem. 268: 601-607.
45. Lou C, Li Z, Ouyang Q,. 2008. A molecular model for persister in E. coli. J. Theor. Biol. 255: 205-209.
46. McQuarrie DA,. 1976. Statistical mechanics. Harper & Row: New York.
47. Moyed HS, Bertrand KP,. 1983. hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J. Bacteriol. 155: 768-775.
48. Moyed HS, Broderick SH,. 1986. Molecular cloning and expression of hipA, a gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J. Bacteriol. 166: 399-403.
49. Oehme DP, Brownlee RT, Wilson DJ,. 2012. Effect of atomic charge, solvation, entropy, and ligand protonation state on MM-PB(GB)SA binding energies of HIV protease. J. Comput. Chem. 33: 2566-2580.
50. Pearlman DA,. 2005. Evaluating the molecular mechanics Poisson-Boltzmann surface area free energy method using a congeneric series of ligands to p38 MAP kinase. J. Med. Chem. 48: 7796-7807.
51. Perez A, Marchan I, Svozil D, Sponer J, Cheatham TE, 3rd, Laughton CA, Orozco M,. 2007. Refinement of the AMBER force field for nucleic acids: improving the description of alpha/gamma conformers. Bioph. J. 92: 3817-3829.
52. Rotem E, Loinger A, Ronin I, Levin-Reisman I, Gabay C, Shoresh N, Biham O, Balaban NQ,. 2010. Regulation of phenotypic variability by a threshold-based mechanism underlies bacterial persistence. Proc. Natl. Acad. Sci. U.S.A. 107: 12541- 12546.
53. Sadiq SK, De Fabritiis G,. 2010. Explicit solvent dynamics and energetics of HIV-1 protease flap opening and closing. Proteins 78: 2873-2885.
54. Scherrer R, Moyed HS,. 1988. Conditional impairment of cell division and altered lethality in hipA mutants of Escherichia coli K-12. J. Bacteriol. 170: 3321-3326.
55. Schumacher MA, Piro KM, Xu W, Hansen S, Lewis K, Brennan RG,. 2009. Molecular mechanisms of HipA-mediated multidrug tolerance and its neutralization by HipB. Science 323: 396-401.
56. Shah D, Zhang Z, Khodursky A, Kaldalu N, Kurg K, Lewis K,. 2006. Persisters: a distinct physiological state of E. coli. BMC Microbiol. 6: 53.
57. Simard JR, Pawar V, Aust B, Wolf A, Rabiller M, Wulfert S, Robubi A, Klüter S, Ottmann C, Rauh D,. 2009. High-throughput screening to identify inhibitors which stabilize inactive kinase conformations in p38α. J. Am. Chem. Soc. 131: 18478- 18488.
58. Stoica I, Sadiq SK, Coveney PV,. 2008. Rapid and accurate prediction of binding free energies for saquinavir-bound HIV-1 proteases. J. Am. Chem. Soc. 130: 2639-2648.
59. Strahs D, Schlick T,. 2000. A-tract bending: insights into experimental structures by computational models. J. Mol. Biol. 301: 643-664.
60. Vazquez-Laslop N, Lee H, Neyfakh AA,. 2006. Increased persistence in Escherichia coli caused by controlled expression of toxins or other unrelated proteins. J. Bacteriol. 188: 3494-3497.
61. Wang J, Morin P, Wang W, Kollman PA,. 2001. Use of MM-PBSA in reproducing the binding free energies to HIV-1 RT of TIBO derivatives and predicting the binding mode to HIV-1 RT of efavirenz by docking and MM-PBSA. J. Am. Chem. Soc. 123: 5221-5230.