Insights into the thermal stabilization and conformational transitions of DNA by hyperthermophile protein Sso7d: Molecular dynamics simulations and MM-PBSA analysis

Journal of Biomolecular Structure and Dynamics

Volumn 30, Issue 6, 2012, Pages 716-727

  Chen, Lin ^a   Zheng, Qing Chuan ^a   Yu, Li Ying ^a   Chu, Wen Ting ^a   Zhang, Ji Long ^a   Xue, Qiao ^a   Zhang, Hong Xing ^a   Sun, Chia Chung ^a  

^a JILIN UNIVERSITY   (China)

Author keywords

DNA kinking; Hyperthermophile; MM PBSA; Molecular dynamics; Protein DNA interaction; Structural transitions; Thermal stability

Indexed keywords

DOUBLE STRANDED DNA; PROTEIN; PROTEIN SSO7D; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ARTICLE; CONFORMATIONAL TRANSITION; DNA PROTEIN COMPLEX; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; POISSON BOLTZMANN SURFACE AREA ANALYSIS; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN STRUCTURE; TEMPERATURE; THERMOSTABILITY;

ARCHAEAL PROTEINS; DNA-BINDING PROTEINS; GC RICH SEQUENCE; MOLECULAR DYNAMICS SIMULATION; NUCLEIC ACID CONFORMATION; OLIGODEOXYRIBONUCLEOTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SURFACE PROPERTIES; THERMODYNAMICS;

EID: 84867632652     PISSN: 07391102     EISSN: 15380254     Source Type: Journal    
DOI: 10.1080/07391102.2012.689702     Document Type: Article

References (59)

1. Agha-Amiri, K., & Klein, A. (1993). Nucleotide sequence of a gene encoding a histone-like protein in the archaeon Methanococcus voltae. Nucleic Acids Research, 21, 1491.
2. Arnott, S., & Hukins, D.W.L. (1972). Optimised parameters for A-DNA and B-DNA. Biochemical and Biophysical Research Communications, 47, 1504-1509.
3. Arora, N., & Jayaram, B. (1998). Energetics of base pairs in BDNA in solution: An appraisal of potential functions and dielectric treatments. The Journal of Physical Chemistry B, 102, 6139-6144.
4. Bashford, D., & Case, D.A. (2000). Generalized born models of macromolecular salvation effects. Annual Review of Physical Chemistry, 51, 129-152.
5. Baumann, H., Knapp, S., Karshikoff, A., Ladenstein, R., & Hard, T. (1995). DNA-binding surface of the Sso7d protein from Sulfolobus solfataricus. Journal of Molecular Biology, 247, 840-846.
6. Baumann, H., Knapp, S., Lundback, T., Ladenstein, R., & Hard, T. (1994). Solution structure and DNA-binding properties of a thermostable protein from the archaeon Sulfolobus solfataricus. Natural Structural Biology, 1, 808-819.
7. Bernini, A., Spiga, O., Consonni, R., Arosio, I., Fusi, P., Cirri, S.,Niccolai, N. (2011). Hydration studies on the archaeal protein Sso7d using NMR measurements and MD simulations. BMC Structural Biology, 11, 44.
8. Bueren-Calabuig, J.A., Giraudon, C., Galmarini, C.M., Egly, J. M., & Gago, F. (2011). Temperature-induced melting of double-stranded DNA in the absence and presence of covalently bonded antitumour drugs: Insight from molecular dynamics simulations. Nucleic Acids Research, 39, 8248-8257.
9. Case, D.A., Darden, T.A., Cheatham III, T.E., Simmerling, C. L., Wang, J., Duke, R.E., Kollman, P.A. (2008). AMBER10. San Francisco, CA: University of California.
10. Case, D.A., Darden, T.A., Cheatham III, T.E., Simmerling, C. L., Wang, J., Duke, R.E., Kollman, P.A. (2010). AMBER11. San Francisco, CA: University of California.
11. Choli, T., Henning, P., Wittmann-Liebold, B., & Reinhardt, R. (1988). Isolation, characterization, and microsequence analysis of a small basic methylated DNA-binding protein from the Archaebacterium Sulfolobus solfataricus. Biochimica et Biophysica Acta, 950, 193-203.
12. Cremer, D., & Pople, J.A. (1975). A general definition of ring puckering coordinates. Journal of the American Chemical Society, 97, 1354-1358.
13. Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N. log(N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98, 10089-10092.
14. Delano, W.L. (2002). The PyMOL molecular graphics system and users manual. San Carlos, CA: Delano scientific.
15. Dostal, L., Chen, C.Y., Wang, A.H.J., & Welfle, H. (2004). Partial B-To-A DNA transition upon minor groove binding of protein Sac7d monitored by Raman Spectroscopy. Biochemistry, 43, 9600-9609.
16. Duan, Y., Wu, C., Chowdhury, S., Lee, M.C., Xiong, G., Zhang, W.,Kollman, P. (2003). A point-charge force field for molecular mechanics simulations of protein based on condensed-phase quantum mechanical calculations. Journal of Computational Chemistry, 24, 1999-2012.
17. Gao, Y.G., Su, S.Y., Robinson, H., Padmanabhan, S., Lim, L., McCrary, B.S., Wang, A.H. (1998). The crystal structure of the hyperthermophile chromosomal protein Sso7d bound to DNA. Nature Structural Biology, 5, 782-786.
18. Gera, N., Hussain, M., Wright, R.C., & Rao, B.M. (2011). Highly stable binding proteins derived from the hyperthermophilic Sso7d scaffold. Journal of Molecular Biology, 409, 601-616.
19. Gorfe, A.A., & Jelesarov, I. (2003). Energetics of sequencespecific protein-DNA association: Computational analysis of integrase Tn916 binding to its target DNA. Biochemistry, 42, 11568-11576.
20. Gouda, H., Kuntz, I.D., Case, D.A., & Kollman, P.A. (2003). Free energy calculations for theophylline binding to an RNA aptamer: Comparison of MM-PBSA and thermodynamic integration methods. Biopolymers, 68, 16-34.
21. Guagliardi, A., Napoli, A., Rossi, M., & Ciaramella, M. (1997). Annealing of complementary DNA strands above the melting point of the duplex promoted by an archaeal protein. Journal of Molecular Biology, 267, 841-848.
22. Habtemariam, B., Anisimov, V.M., & MacKerell, A.D.J. (2005). Cooperative binding of DNA and CBFβ to the runt domain of the CBFα studied via MD simulations. Nucleic Acids Research, 33, 4212-4222.
23. Hardy, C.D., & Martin, P.K. (2008). Biochemical characterization of DNA-binding proteins from Pyrobaculum aerophilum and Aeropyrum pernix. Extremophiles, 12, 235-246.
24. Harvey, S.C., & Prabhakaran, M. (1986). Ribose puckering: Structure, dynamics, energetics, and the pseudorotation cycle. Journal of the American Chemical Society, 108, 6128-6136.
25. Hou, T.J., Wang, J.M., Li, Y.Y., & Wang, W. (2011). Assessing the performance of the MM/PBSA and MM/GBSA methods. I. The accuracy of binding free energy calculations based on molecular dynamics simulations. Journal of Chemical Information and Modeling, 51, 69-82.
26. Humphery, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14, 33-38.
27. Jayaram, B., McConnell, K., Dixit, S.B., Das, A., & Beveridge, D.L. (2002). Free-Energy component analysis of 40 protein-DNA complexes: A consensus view on the thermodynamics of binding at the molecular level. Journal of Computational Chemistry, 23, 1-14.
28. Knapp, S., Karshikoff, A., Berndt, K.D., Christova, P., Atanasov, B., & Ladenstein, R. (1996). Thermal unfolding of the DNA-binding protein Sso7d from the hyperthermophile Sulfolobus solfataricus. Journal of Molecular Biology, 264, 1132-1144.
29. Lee, H.M., Jin, B., Han, S.W., & Kim, S.K. (2010). Conformational analysis of genotoxic benzo[α]pyrene-7, 8-dione-duplex DNA adducts using a molecular dynamics method (II). Journal of Biomolecular Structure & Dynamics, 28, 421-430.
30. Lee, J., Kim, J.S., & Seok, C. (2010). Cooperativity and specificity of Cys2His2 Zinc finger protein-DNA interactions: A molecular dynamics simulation study. The Journal of Physical Chemistry B, 114, 7662-7671.
31. Leroy, J.L., Kochoyan, M., Huynh-Dinh, T., & Gueron, M. (1988). Characterization of base-pair opening in deoxynucleotide duplexes using catalyzed exchange of the imino proton. Journal of Molecular Biology, 200, 223-238.
32. Lopez-Garcia, P., Knapp, S., Ladenstein, R., & Forterre, P. (1998). In vitro DNA binding of the archaeal protein Sso7d induces negative supercoiling at temperatures typical thermophilic growth. Nucleic Acids Research, 26, 2322-2328.
33. Lundback, T., Hansson, H., Knapp, S., Ladenstein, R., & Hard, T. (1998). Thermodynamic characterization of nonsequence-specific DNA-binding by the Sso7d protein from Sulfolobus solfataricus. Journal of Molecular Biology, 276, 775-786.
34. Lundback, T., & Hard, T. (1996). Salt dependence of the free energy, enthalpy, and entropy of nonsequence specific DNA binding. The Journal of Physical Chemistry, 100, 17690-17695.
35. Luo, R., David, L., & Gilson, M.K. (2002). Accelerated Poisson-Boltzmann calculations for static and dynamic systems. Journal of Computational Chemistry, 23, 1244-1253.
36. Luscombe, N.M., Austin, S.E., Berman, H.M., & Thornton, J. M. (2000). An overview of the structures of protein-DNA complexes. Genome Biology, 1, 1-37.
37. MacKerell, A.D.J., & Nilsson, L. (2008). Molecular dynamics simulations of nucleic acid-protein complexes. Current Opinion in Structural Biology, 18, 194-199.
38. Marathe, A., & Bansal, M. (2010). The 5-methyl group in thymine dynamically influences the structure of A-Tracts in DNA at the local and global level. The Journal of Physical Chemistry B, 114, 5534-5546.
39. McAfee, J.G., Edmondson, S.P., Datta, P.K., Shriver, J.W., & Gupta, R. (1995). Gene cloning, expression, and characterization of the Sac7 proteins from the Hyperthermophile Sulfolobus acidocaldarius. Biochemistry, 34, 10063-10077.
40. Merlino, A., Graziano, G., & Mazzarella, L. (2004). Structural and dynamic effects of α-helix deletion in Sso7d: Implications for protein thermal stability. Proteins: Structure, Function, and Bioinformatics, 57, 692-701.
41. Napoli, A., Zivanovic, Y., Bocs, C., Buhler, C., Rossi, M., Forterre, P., & Ciaramella, M. (2002). DNA bending, compaction and negative supercoiling by the architectural protein Sso7d of Sulfolobus solfataricus. Nucleic Acids Research, 30, 2656-2662.
42. Nasiri, R., Bahrami, H., Zahedi, M., Moosavi-Movahedi, A.A., & Sattarahmdy, N. (2010). A theoretical elucidation of glucose interaction with HAS's domains. Journal of Biomolecular Structure & Dynamics, 28, 211-226.
43. Nonin, S., Leroy, J.L., & Gueron, M. (1995). Terminal base pairs of oligodeoxynucleotides: Imino proton exchange and fraying. Biochemistry, 34, 10652-10659.
44. Peters, W.B., Edmondson, S.P., & Shriver, J.W. (2004). Thermodynamics of DNA binding and distortion by the hyperthermophile chromation protein Sac7d. Journal of Molecular Biology, 343, 339-360.
45. Priyakumar, U.D. (2012). Role of hydrophobic core on the thermal stability of proteins-molecular dynamics simulations on the single point mutant of Sso7d. Journal of Biomolecular Structure & Dynamics, 29, 961-971.
46. Priyakumar, U.D., Harika, G., & Suresh, G. (2010). Molecular simulations on the thermal stabilization of DNA by Hyperthermophilic chromatin protein Sac7d, and associated conformational transitions. The Journal of Physical Chemistry B, 114, 16548-16557.
47. Priyakumar, U.D., Ramakrishna, S., Nagarjuna, K.R., & Reddy, S.K. (2010). Structural and energetic determinants of thermal stability and hierarchical unfolding pathways of Hyperthermophilic proteins, Sac7d and Sso7d. The Journal of Physical Chemistry B, 114, 1707-1718.
48. Ren, Y., Gao, J., Ge, W., & Li, J.-H. (2009). Thermal unfolding of a double-domain protein: Molecular dynamics simulation of Rhodanese. Industrial & Engineering Chemistry Research, 48, 8865-8871.
49. Reyes, C.M., & Kollman, P.A. (2000). Structure and thermodynamics of RNA-protein binding: Using molecular dynamics and free energy analyses to calculate the free energies of binding and conformational change. Journal of Molecular Biology, 297, 1145-1158.
50. Ryckaert, J.P., Ciccotti, G., & Berendsen, H.J.C. (1977). Numerical integration of the Cartesian equations of motion of a system with constraints: Molecular dynamics of nalkanes. Journal of Computational Physics, 23, 327-341.
51. Saenger, W. (1984). Principles of nucleic acid structure. New York, NY: Springer-Verlag.
52. Sklenovsky, P., & Otyepka, M. (2010). In silico structural and functional analysis of fragments of the Ankyrin repeat protein p18INK4c. Journal of Biomolecular Structure & Dynamics, 27, 521-540.
53. Srinivasan, J., Cheatham, T.E., Cieplak, P., Kollman, P.A., & Case, D.A. (1998). Continuum solvent studies of the stability of DNA, RNA, and phosphoramidate-DNA helixes. Journal of the American Chemical Society, 120, 9401-9409.
54. Swanson, J.M., Henchman, R.H., & McCammon, J.A. (2004). Revisiting free energy calculations: A theoretical connection to MM/PBSA and direct calculation of the association free energy. Biophysical Journal, 86, 67-74.
55. Tolstorukov, M.Y., Jernigan, R.L., & Zhurkin, V.B. (2004). Protein-DNA hydrophobic recognition in the minor groove is facilitated by sugar switching. Journal of Molecular Biology, 337, 65-76.
56. Wiesner, J., Kriz, Z., Kuca, K., Jun, D., & Koca, J. (2010). Influence of the acetylcholinesterase active site protonation on omega loop and active site dynamics. Journal of Biomolecular Structure & Dynamics, 28, 393-403.
57. Xu, X., Su, J., Chen, W., & Wang, C. (2011). Thermal stability and unfolding pathways of Sso7d and its mutant F31A: Insight from molecular dynamics simulation. Journal of Biomolecular Structure & Dynamics, 28, 717-727.
58. Yang, B., Zhu, Y., Wang, Y., & Chen, G. (2011). Interaction identification of ZIF268 and TATAZF proteins with GC-/AT-rich DNA sequence: A theoretical study. Journal of Computational Chemistry, 32, 416-428.
59. Zhang, Q., & Schlick, T. (2006). Stereochemistry and positiondependent effects of carcinogens on TATA/TBP binding. Biophysical Journal, 90, 1865-1877.