Conformational changes and allosteric communications in human serum albumin due to ligand binding

Journal of Biomolecular Structure and Dynamics

Volumn 33, Issue 10, 2015, Pages 2192-2204

  Ahalawat, Navjeet ^a   Murarka, Rajesh K ^a  

^a INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH BHOPAL   (India)

Author keywords

allostery; dynamic network analysis; elastic network model; human serum albumin; principal component analysis; statistical coupling analysis; X ray ensemble

Indexed keywords

HUMAN SERUM ALBUMIN; FATTY ACID; LIGAND; PROTEIN BINDING; SERUM ALBUMIN;

ALLOSTERISM; ARTICLE; BINDING AFFINITY; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; INTERMETHOD COMPARISON; LIGAND BINDING; MATHEMATICAL MODEL; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; CHEMISTRY; HUMAN; MOLECULAR DYNAMICS; MOTION; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

ALLOSTERIC SITE; CRYSTALLOGRAPHY, X-RAY; FATTY ACIDS; HUMANS; LIGANDS; MOLECULAR DYNAMICS SIMULATION; MOTION; PROTEIN BINDING; PROTEIN CONFORMATION; SERUM ALBUMIN; THERMODYNAMICS;

EID: 84938980436     PISSN: 07391102     EISSN: 15380254     Source Type: Journal    
DOI: 10.1080/07391102.2014.996609     Document Type: Article

References (73)

1. Ahmed, A., Villinger, S., and, Gohlke, H. (2010). Large-scale comparison of protein essential dynamics from molecular dynamics simulations and coarse-grained normal mode analyses. Proteins: Structure, Function, and Bioinformatics, 78, 3341-3352.
2. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and, Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25, 3389-3402. 10.1093/nar/25.17.3389
3. Ascenzi, P., Bocedi, A., Notari, S., Menegatti, E., and, Fasano, M. (2005). Heme impairs allosterically drug binding to human serum albumin sudlows site I. Biochemical and Biophysical Research Communications, 334, 481-486. 10.1016/j.bbrc.2005.06.127
4. Ascenzi, P., and, Fasano, M. (2010). Allostery in a monomeric protein: The case of human serum albumin. Biophysical Chemistry, 148, 16-22. 10.1016/j.bpc.2010.03.001
5. Atilgan, A. R., Durell, S. R., Jernigan, R. L., Demirel, M. C., Keskin, O., and, Bahar, I. (2001). Anisotropy of fluctuation dynamics of proteins with an elastic network model. Biophysical Journal, 80, 505-515. 10.1016/S0006-3495(01)76033-X
6. Bahar, I., Atilgan, A. R., Demirel, M. C., and, Erman, B. (1998). Vibrational dynamics of folded proteins: Significance of slow and fast motions in relation to function and stability. Physical Review Letters, 80, 2733-2736. 10.1103/PhysRevLett.80.2733
7. Bahar, I., Lezon, T. R., Bakan, A., and, Shrivastava, I. H. (2010). Normal mode analysis of biomolecular structures: Functional mechanisms of membrane proteins. Chemical Reviews, 110, 1463-1497.
8. Bahar, I., Lezon, T. R., Yang, L. W., and, Eyal, E. (2010). Global dynamics of proteins: Bridging between structure and function. Annual Review of Biophysics, 39, 23-42.
9. Bakan, A., and, Bahar, I. (2009). The intrinsic dynamics of enzymes plays a dominant role in determining the structural changes induced upon inhibitor binding. Proceedings of the National Academy of Sciences, 106, 14349-14354. 10.1073/pnas.0904214106
10. Berendsen, H. J. C., Postma, J. P. M., Vangunsteren, W. F., Dinola, A., and, Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81, 3684-3690. 10.1063/1.448118
11. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H.,., Bourne, P. E. (2000). The protein data bank. Nucleic Acids Research, 28, 235-242. 10.1093/nar/28.1.235
12. Best, R. B., Lindorff-Larsen, K., DePristo, M. A., and, Vendruscolo, M. (2006). Relation between native ensembles and experimental structures of proteins. Proceedings of the National Academy of Sciences, 103, 10901-10906. 10.1073/pnas.0511156103
13. Bhattacharya, A. A., Grune, T., and, Curry, S. (2000). Crystallographic analysis reveals common modes of binding of medium and long-chain fatty acids to human serum albumin. Journal of Molecular Biology, 303, 721-732. 10.1006/jmbi.2000.4158
14. Boehr, D. D., Nussinov, R., and, Wright, P. E. (2009). The role of dynamic conformational ensembles in biomolecular recognition. Nature Chemical Biology, 5, 789-796. 10.1038/nchembio.232
15. Bussi, G., Donadio, D., and, Parrinello, M. (2007). Canonical sampling through velocity rescaling. Journal of Chemical Physics, 126, 014101.
16. Curry, S. (2009). Lessons from the crystallographic analysis of small molecule binding to human serum albumin. Drug Metabolism and Pharmacokinetics, 24, 342-357. 10.2133/dmpk.24.342
17. Curry, S., Mandelkow, H., Brick, P., and, Franks, N. (1998). Crystal structure of human serum albumin complexed with fatty acid reveals an asymmetric distribution of binding sites. Nature Structural Biology, 5, 827-835. 10.1038/1869
18. Darden, T., York, D., and, Pedersen, L. (1993). Particle mesh Ewald: An Nslog(N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98, 10089-10092. 10.1063/1.464397
19. Eargle, J., and, Luthey-Schulten, Z. (2012). NetworkView: 3D display and analysis of protein. RNA interaction networks. Bioinformatics, 28, 3000-3001. 10.1093/bioinformatics/bts546
20. Edgar, R. C. (2004). Muscle: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792-1797. 10.1093/nar/gkh340
21. Emekli, U., Schneidman-Duhovny, D., Wolfson, H. J., Nussinov, R., and, Haliloglu, T. (2008). HingeProt: Automated prediction of hinges in protein structures. Proteins-Structure Function and Bioinformatics, 70, 1219-1227.
22. Fanali, G., di Masi, A., Trezza, V., Marino, M., Fasano, M., and, Ascenzi, P. (2012). Human serum albumin: From bench to bedside. Molecular Aspects of Medicine, 33, 209-290. 10.1016/j.mam.2011.12.002
23. Fanali, G., Pariani, G., Ascenzi, P., and, Fasano, M. (2009). Allosteric and binding properties of Asp1-Glu382 truncated recombinant human serum albumin-An optical and NMR spectroscopic investigation. FEBS Journal, 276, 2241-2250. 10.1111/ejb.2009.276.issue-8
24. Frauenfelder, H., Sligar, S. G., and, Wolynes, P. G. (1991). The energy landscapes and motions of proteins. Science, 254, 1598-1603.
25. Fujiwara, S., and, Amisaki, T. (2008). Identification of high affinity fatty acid binding sites on human serum albumin by MM-PBSA method. Biophysical Journal, 94, 95-103. 10.1529/biophysj.107.111377
26. Ghuman, J., Zunszain, P. A., Petitpas, I., Bhattacharya, A. A., Otagiri, M., and, Curry, S. (2005). Structural basis of the drug-binding specificity of human serum albumin. Journal of Molecular Biology, 353, 38-52. 10.1016/j.jmb.2005.07.075
27. Haliloglu, T., Keskin, O., Ma, B. Y., and, Nussinov, R. (2005). How similar are protein folding and protein binding nuclei? Examination of vibrational motions of energy hot spots and conserved residues. Biophysical Journal, 88, 1552-1559. 10.1529/biophysj.104.051342
28. Hess, B., Bekker, H., Berendsen, H. J. C., and, Fraaije, J. G. E. M. (1997). Lincs: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18, 1463-1472. 10.1002/(ISSN)1096-987X
29. Henzler-Wildman, K., and, Kern, D. (2007). Dynamic personalities of proteins. Nature, 450, 964-972.
30. Hinsen, K. (1998). Analysis of domain motions by approximate normal mode calculations. Proteins: Structure, Function, and Genetics, 33, 417-429. 10.1002/(ISSN)1097-0134
31. Horn, H. W., Swope, W. C., Pitera, J. W., Madura, J. D., Dick, T. J., Hura, G. L., and, Head-Gordon, T. (2004). Development of an improved four-site water model for biomolecular simulations: TIP4P-Ew. The Journal of Chemical Physics, 120, 9665-9678. 10.1063/1.1683075
32. Humphrey, W., Dalke, A., and, Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14, 27-38.
33. Jana, B., Adkar, B. V., Biswas, R., and, Bagchi, B. (2011). Dynamic coupling between the LID and NMP domain motions in the catalytic conversion of ATP and AMP to ADP by adenylate kinase. The Journal of Chemical Physics, 134, 035101.
34. Koshland, D. E. (1958). Application of a theory of enzyme specificity to protein synthesis. Proceedings of the National Academy of Sciences, 44, 98-104. 10.1073/pnas.44.2.98
35. Krenzel, E. S., Chen, Z., and, Hamilton J. A. (2013). Correspondence of fatty acid and drug binding sites on human serum albumin: A two-dimensional nuclear magnetic resonance study. Biochemistry, 52, 1559-1567. 10.1021/bi301458b
36. Kundu, S., Sorensen, D. C., and, Phillips, G. N. (2004). Automatic domain decomposition of proteins by a Gaussian network model. Proteins-Structure Function and Bioinformatics, 57, 725-733. 10.1002/(ISSN)1097-0134
37. Lange, O. F., and, Grubmuller, H. (2006). Generalized correlation for biomolecular dynamics. Proteins, 62, 1053-1061.
38. Lange, O. F., Lakomek, N. A., Fares, C., Schroder, G. F., Walter, K. F., Becker, S.,., de Groot, B. L. (2008). Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science, 320, 1471-1475.
39. Lockless, S. W., and, Ranganathan, R. (1999). Evolutionarily conserved pathways of energetic connectivity in protein families. Science, 286, 295-299. 10.1126/science.286.5438.295
40. Ma, B., Kumar, S., Tsai, C. J., and, Nussinov, R. (1999). Folding funnels and binding mechanisms. Protein Engineering Design and Selection, 12, 713-720. 10.1093/protein/12.9.713
41. Miyamoto, S., and, Kollman, P. A. (1992). Settle: An analytical version of the shake and rattle algorithm for rigid water models. Journal of Computational Chemistry, 13, 952-962. 10.1002/(ISSN)1096-987X
42. Monod, J., Wyman, J., and, Changeux, J. P. (1965). On the nature of allosteric transitions: A plausible model. Journal of Molecular Biology, 12, 88-118. 10.1016/S0022-2836(65)80285-6
43. Orellana, L., Rueda, M., Ferrer-Costa, C., Lopez-Blanco, J. R., Chacon, P., and, Orozco, M. (2010). Approaching elastic network models to molecular dynamics flexibility. Journal of Chemical Theory and Computation, 6, 2910-2923. 10.1021/ct100208e
44. Parrinello, M., and, Rahman, A. (1981). Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics, 52, 7182-7190. 10.1063/1.328693
45. Peng, C., and, Head-Gordon, T. (2011). The dynamical mechanism of auto-inhibition of AMP-activated protein kinase. Plos Computational Biology, 7, e1004009.
46. Peng, C., Zhang, L. Q., and, Head-Gordon, T. (2010). Instantaneous normal modes as an unforced reaction coordinate for protein conformational transitions. Biophysical Journal, 98, 2356-2364.
47. Petitpas, I., Grune, T., Bhattacharya, A. A., and, Curry, S. (2001). Crystal structures of human serum albumin complexed with monounsaturated and polyunsaturated fatty acids. Journal of Molecular Biology, 314, 955-960. 10.1006/jmbi.2000.5208
48. Romo, T. D., and, Grossfield, A. (2011). Validating and improving elastic network models with molecular dynamics simulations. Proteins: Structure, Function and Bioinformatics, 79, 23-34.
49. Rueda, M., Chacon, P., and, Orozco, M. (2007). Thorough validation of protein normal mode analysis: A comparative study with essential dynamics. Structure, 15, 565-575.
50. Sanejouand, Y. H. (2013). Elastic network models: Theoretical and empirical foundations. Methods in Molecular Biology, 924, 601-616.
51. Sethi, A., Eargle, J., Black, A. A., and, Luthey-Schulten, Z. (2009). Dynamical networks in tRNA:protein complexes. Proceedings of the National Academy of Sciences, 106, 6620-6625. 10.1073/pnas.0810961106
52. Simard, J. R., Zunszain, P. A., Ha, C. E., Yang, J. S., Bhagavan, N. V., Petitpas, I.,., Hamilton, J. A. (2005). Locating high-affinity fatty acid-binding sites on albumin by X-ray crystallography and NMR spectroscopy. Proceedings of the National Academy of Sciences, 102, 17958-17963. 10.1073/pnas.0506440102
53. Simard, J. R., Zunszain, P. A., Hamilton, J. A., and, Curry, S. (2006). Location of high and low affinity fatty acid binding sites on human serum albumin revealed by NMR drug-competition analysis. Journal of Molecular Biology, 361, 336-351. 10.1016/j.jmb.2006.06.028
54. Skjaerven, L., Martinez, A., and, Reuter, N. (2011). Principal component and normal mode analysis of proteins; a quantitative comparison using the GroEL subunit. Proteins: Structure, Function and Bioinformatics, 79, 232-243.
55. Smock, R. G., and, Gierasch, L. M. (2009). Sending signals dynamically. Science, 324, 198-203.
56. Smock, R. G., Rivoire, O., Russ, W. P., Swain, J. F., Leibler, S., Ranganathan, R., and, Gierasch, L. M. (2010). An interdomain sector mediating allostery in Hsp70 molecular chaperones. Molecular Systems Biology, 6, 414.
57. Sudhamalla, B., Gokara, M., Ahalawat, N., Amooru, D. G., and, Subramanyam, R. (2010). Molecular dynamics simulation and binding studies of β-sitosterol with human serum albumin and its biological relevance. The Journal of Physical Chemistry B, 114, 9054-9062. 10.1021/jp102730p
58. Suel, G. M., Lockless, S. W., Wall, M. A., and, Ranganathan, R. (2003). Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nature Structural Biology, 10, 59-69. 10.1038/nsb881
59. Sugio, S., Kashima, A., Mochizuki, S., Noda, M., and, Kobayashi, K. (1999). Crystal structure of human serum albumin at 2.5 A resolution. Protein Engineering Design and Selection, 12, 439-446. 10.1093/protein/12.6.439
60. Tama, F., and, Brooks, C. L. (2006). Symmetry, form, and shape: guiding principles for robustness in macromolecular machines. Annual Review of Biophysics and Biomolecular Structure, 35, 115-133.
61. Tama, F., Gadea, F. X., Marques, O., and, Sanejouand, Y. H. (2000). Building-block approach for determining low-frequency normal modes of macromolecules. Proteins-Structure Function and Genetics, 41, 1-7. 10.1002/(ISSN)1097-0134
62. Tokuriki, N., and, Tawfik, D. S. (2009). Protein dynamism and evolvability. Science, 324, 203-207.
63. Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., and, Berendsen, H. J. (2005). Gromacs: Fast, flexible, and free. Journal of Computational Chemistry, 26, 1701-1718. 10.1002/(ISSN)1096-987X
64. Vanwart, A. T., Eargle, J., Luthey-Schulten, Z., and, Amaro, R. E. (2012). Exploring residue component contributions to dynamical network models of allostery. Journal of Chemical Theory and Computation, 8, 2949-2961. 10.1021/ct300377a
65. Wang, J., Wang, W., Kollman, P. A., and, Case, D. A. (2006). Automatic atom type and bond type perception in molecular mechanical calculations. Journal of Molecular Graphics and Modelling, 25, 247-260. 10.1016/j.jmgm.2005.12.005
66. Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., and, Case, D. A. (2004). Development and testing of a general amber force field. Journal of Computational Chemistry, 25, 1157-1174. 10.1002/(ISSN)1096-987X
67. Yang, L., Song, G., Carriquiry, A., and, Jernigan, R. L. (2008). Close correspondence between the motions from principal component analysis of multiple HIV-1 protease structures and elastic network modes. Structure, 16, 321-330. 10.1016/j.str.2007.12.011
68. Yang, L., Song, G., and, Jernigan, R. L. (2007). How well can we understand large-scale protein motions using normal modes of elastic network models? Biophysical Journal, 93, 920-929.
69. Yang, L., Song, G., and, Jernigan, R. L. (2009). Protein elastic network models and the ranges of cooperativity. Proceedings of the National Academy of Sciences, 106, 12347-12352. 10.1073/pnas.0902159106
70. Zheng, W. (2008). A unification of the elastic network model and the Gaussian network model for optimal description of protein conformational motions and fluctuations. Biophysical Journal, 94, 3853-3857. 10.1529/biophysj.107.125831
71. Zheng, W. J., Brooks, B. R., and, Thirumalai, D. (2006). Low-frequency normal modes that describe allosteric transitions in biological nanomachines are robust to sequence variations. Proceedings of the National Academy of Sciences, 103, 7664-7669.
72. Zunszain, P. A., Ghuman, J., Komatsu, T., Tsuchida, E., and, Curry, S. (2003). Crystal structural analysis of human serum albumin complexed with hemin and fatty acid. BMC Structural Biology, 3, 1-9.
73. Zunszain, P. A., Ghuman, J., McDonagh, A. F., and, Curry, S. (2008). Crystallographic analysis of human serum albumin complexed with 4Z,15E-bilirubin-IXα. Journal of Molecular Biology, 381, 394-406. 10.1016/j.jmb.2008.06.016